ALL PUBLICATIONS

• ​​Jonas Malkmus, Angela Morabito, Lucille Lopez-Delisle, Laura Avino-Esteban, Alexandre Mayran, Aimee Zuniga, James Sharpe, Rolf Zeller, Rushikesh Sheth (2025); WNT signaling coordinately controls mouse limb bud outgrowth and establishment of the digit-interdigit pattern. Development 1 June 2025; 152 (11): dev204606. doi: https://doi.org/10.1242/dev.204606

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• Palacio, V., Pancho, A., Morabito, A. et al. Single-cell profiling of penta- and tetradactyl mouse limb buds identifies mesenchymal progenitors controlling digit numbers and identities. Nat Commun 16, 1226 (2025). https://doi.org/10.1038/s41467-025-56221-1

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• Geoffrey Soussi, Ausra Girdziusaite, Shalu Jhanwar, Victorio Palacio, Marco Notaro, Rushikesh Sheth, Rolf Zeller, Aimée Zuniga (2024). TBX3 is essential for establishment of the posterior boundary of anterior genes and upregulation of posterior genes together with HAND2 during the onset of limb bud development. Development 1 June 2024; 151 (11): dev202722. doi: https://doi.org/10.1242/dev.202722

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• Morabito A., Malkmus J., Pancho A., Zuniga A., Zeller R. and Sheth R. (2023). Optimized protocol for whole-mount RNA fluorescent in situ hybridization using oxidation-mediated autofluorescence reduction on mouse embryos. Star Protocols 4. https://doi.org/10.1016/j.xpro.2023.102603

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• Losa, M., Barozzi, I., Osterwalder, M. et al. (2023) A spatio-temporally constrained gene regulatory network directed by PBX1/2 acquires limb patterning specificity via HAND2.Nat Commun 14, 3993. https://doi.org/10.1038/s41467-023-39443-z

 

• Gamart J., Barozzi I., Laurent F., Reinhardt R., Ramos Martins L., Oberholzer T., Visel  A., Zeller R. and Zuniga A. (2021). SMAD4 target genes are part of a transcriptional network that integrates the response to BMP and SHH signaling during early limb bud patterning. Development 148: dev200182.

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• Jhanwar S., Malkmus J, Stolte J., Romashkina O., Zuniga A. and Zeller R. (2021). Conserved and species-specific chromatin remodeling and regulatory dynamics during mouse and chicken limb bud development. Nature Commun 12, 5685.

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• Malkmus J., Ramos-Martins L., Jhanwar S., Kircher B., Palacio V., Sheth R., Leal F., Duchesne A., Lopez-Rios J., Peterson K.A., Reinhardt R., Onimaru K., Cohn M.J., Zuniga A. and Zeller R. (2021). Spatial regulation by multiple Gremlin1 enhancers provides digit development with cis-regulatory robustness and evolutionary plasticity. Nature Commun 12, 5557.

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• Elliott K.H., Chen X, Salomone J., Chaturvedi P., Schultz P.A., Balchand S.K., Servetas J.D., Zuniga A., Zeller R., Gebelein B., Weirauch M.T., Peterson K.A. and Brugmann S.A. (2020). Gli3 utilizes Hand2 to synergistically regulate tissue-specific transcriptional networks. eLife 9, e56450.

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• ​Desanlis I., Kherdjemil Y., Mayran A., Bouklouch Y., Gentile C., Sheth R., Zeller R., Drouin J., Kmita M. (2020). HOX13-dependent chromatin accessibility underlies the transition towards the digit development program. Nat Commun 11, 2491.

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• Tissières V., Geier F., Kessler B., Wolf E., Zeller R. and Lopez-Rios J. (2020). Gene regulatory and expression differences between mouse and pig limb buds provide insights into the evolutionary emergence of artiodactyl traits. Cell Reports 31, 107490.

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• Reinhardt R., Gullotta F., Nusspaumer G., Ünal E., Ivanek R., Zuniga A. and Zeller R. (2019). Molecular signatures identify immature mesenchymal progenitors in early mouse limb buds that respond differentially to morphogen signaling. Development 146, doi: 10.1242/dev.173328

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• Nusspaumer G., Jaiswal S., Barbero A., Reinhardt R., Ronen D.I., Haumer A., Lufkin T., Martin I. and Zeller R. (2017). Ontogenic Identification and Analysis of Mesenchymal Stromal Cell Populations during Mouse Limb and Long Bone Development. , Stem Cell Reports 9, 1124–1138.

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• Laurent F., Girdziusaite A., Gamart J., Barozzi I., Osterwalder M., Akiyama J.A., Lincoln J., Javier Lopez-Rios J., Visel A., Zuniga A. and Zeller R. (2017). HAND2 Target Gene Regulatory Networks Control Atrioventricular Canal and Cardiac Valve Development. Cell Reports 19, 1602-1613.

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• Schmitz-Rohmer D., Probst S., Yang Z.Z., Laurent F., Zuniga A., Zeller R., Hynx D., Hemmings B.A. and Hergovich A. (2015). NDR kinases are essential for somitogenesis and cardiac looping during mouse embryonic development. PLoS One 10, e0136566.

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• Vaillant C., Valdivieso P., Nuciforo S., Kool M., Schwarzentruber-Schauerte A., Méreau H., Cabuy E., Lobrinus J.A., Pfister S., Zuniga A., Frank S. and Zeller R. (2015). Serpine2/PN-1 is required for Proliferative Expansion of Pre-Neoplastic Lesions and Malignant Progression to Medulloblastoma. PLoS One 10, e0124870.

 

• Van Dusen N.J., Casanovas J., Vincentz J.W., Firulli B.A., Osterwalder M., Lopez-Rios J., Zeller R., Zhou B., Grego-Bessa J., De La Pompa J.L., Shou W. and Firulli A.B. (2014). Hand2 is an Essential Regulator for Two Notch-Dependent Functions within the Embryonic Endocardium. Cell Reports 9, 2071-2083.

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• Osterwalder M., Speziale D., Shoukry M., Mohan R., Ivanek R., Kohler M., Beisel C., Wen X., Scales S.J., Christoffels V.M., Visel A., Lopez-Rios J., and Zeller R. (2014). HAND2 Targets Define a Network of Transcriptional Regulators that Compartmentalize the Early Limb Bud Mesenchyme. Dev Cell 31, 345–357.

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• Lopez-Rios J., Duchesne A., Speziale D., Andrey G., Peterson K.A., Germann P., Ünal E., Liu J., Floriot S., Barbey S., Gallard Y., Müller-Gerbl M., Courtney A.D., Klopp C., Rodriguez S., Ivanek R., Beisel C., Wicking C., Iber D., Robert B., McMahon A.P., Duboule D. and Zeller R. (2014). Attenuated sensing of SHH by Ptch1 underlies evolution of bovine limbs. Nature 511, 46-51. (Article)

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• Benazet J.D. and Zeller R. (2013). Dual Requirement of Ectodermal Smad4 During AER Formation and Termination of Feedback Signaling in Mouse Limb Buds. Genesis 51, 660–666.

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• Probst S., Zeller R. and Zuniga A. (2013). The hedgehog target Vlk genetically interacts with Gli3 to regulate chondrocyte differentiation during mouse long bone development. Differentiation 85, 121-130.​​

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• Bénazet J.D., Pignatti E., Nugent A., Unal E., Laurent F. and Zeller R. (2012). Smad4 is required to induce digit ray primordia and to initiate the aggregation and differentiation of chondrogenic progenitors in mouse limb buds. Development 139, 4250-4260. 

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• Zuniga A., Laurent F., Lopez-Rios J., Klasen C. Matt, N. and Zeller R. (2012). Conserved cis-regulatory regions in a large genomic landscape control SHH and BMP-regulated Gremlin1 expression in mouse limb buds. BMC Dev. Biol. 12, 23 doi:10.1186.

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• Itou J., 2, Kawakami H., Quach T., Osterwalder M., Evans S., Zeller R. and Kawakami Y. (2012). Islet1 regulates establishment of the posterior hindlimb-field upstream of the Hand2-Shh morpho-regulatory network in the mouse. Development 139, 1620-1629.

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• Lopez-Rios J., Speziale D., Robay D., Scotti M., Nusspaumer G., Osterwalder M., Galli A., Holländer G.A., Kmita M. and Zeller R (2012). GLI3 Constrains Digit Number by Controlling Both Progenitor Proliferation and BMP-Dependent Exit to Chondrogenesis. Dev. Cell 22, 837-848. 

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• Gonçalves A. and Zeller R. (2011). Genetic Analysis Reveals an Unexpected Role of BMP7 in Initiation of Ureteric Bud Outgrowth in Mouse Embryos. PLoS One 6, e19370. 

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• Probst S., Kraemer C., Demougin P., Sheth R., Martin G.R., Shiratori H., Hamada H., Iber D., Zeller R. and Zuniga A. (2011) SHH propagates distal limb bud development by enhancing CYP26b1-mediated retinoic acid clearance via AER-FGF signalling. Development 138, 1913-1923.

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• Osterwalder M., Galli A., Rosen B., Skarnes W.C., Zeller R.* and Lopez-Rios J.* (2010, *joint senior authors). Dual RMCE permits high-throughput re-engineering of mutant alleles in mouse ES cells. Nature Methods 7, 893-895.

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• Fujimori S., Novak H., Weissenböck M., Jussila M., Gonçalves A., Zeller R., Galloway J., Thesleff I. and Hartmann C. (2010). Wnt/β-catenin signaling in the dental mesenchyme regulates incisor development by regulating Bmp4. Dev. Biol. 348, 97-106. 

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• Scotti C., Tonnarelli B., Papadimitropoulos A., Scherberich A., Schaeren S., Schauerte A., Lopez-Rios J., Zeller R., Barbero A. and Martin I. (2010). Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc. Natl. Acad. Sci. USA 107, 7251–7256. 

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• Galli A., Robay D., Osterwalder M., Bao X., Bénazet J.D., Tariq M., Paro R., Mackem S. and Zeller R. (2010). Distinct Roles of Hand2 in Initiating Polarity and Posterior Shh Expression during the Onset of Mouse Limb Bud Development. PLoS Genetics 6, e1000901.

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• Bénazet J.D, Bischofberger M., Tiecke E., Gonçalves A, Martin J.F., Zuniga A., Naef F. and Zeller R. (2009). A Self-Regulatory System of Interlinked Signaling Feedback Loops Controls Mouse Limb Patterning. Science 323, 1050-1053.

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• Paparidis, Z., Abbasi, A.A., Malik, S., Goode D.K., Callaway, H., Elgar, G., de Graaff, E., Lopez-Rios, J., Zeller, R. and Grzeschik, K-H. (2007). An ultraconserved non-coding sequence element controls a subset of spatiotemporal GLI3 expression. Dev. Growth Diff. 49, 543-553.

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• Michos O., Gonçalves A., Lopez-Rios J., Tiecke E., Naillat F., Beier K., Galli A., Vainio S. and Zeller, R. (2007). Reduction of BMP4 activity by Gremlin1 enables ureteric bud outgrowth and GDNF/Wnt11 feedback signalling during kidney branching morphogenesis. Development 134, 2397-2405.

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• Vaillant C., Michos O., Brellier F., Orolicki S., Taieb S., Moreno E., Te H., Zeller R. and Monard D. (2007). Protease Nexin-1 and its receptor LRP modulate SHH signalling during cerebellar development. Development 134, 1745-1754.

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• Panman L., Galli A., Lagarde N., Michos O., Soete G., Zuniga A. and Zeller R. (2006). Differential regulation of gene expression in the digit forming area of the mouse limb bud by SHH and Gremlin1/FGF-mediated epithelial-mesenchymal signalling. Development 133, 3419-3428.

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• Panman L., Drenth T., te Welscher P., Zuniga A. and Zeller R. (2005). Genetic interaction of Gli3 and Alx4 during limb development. Int. J. Dev. Bio. 49, 443-448. 

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• Zuniga A, Michos O., Spitz F., Haramis A.P.G., Panman L., Vintersten K., Klasen C., Mansfield W., Kuc S., Duboule D., Dono R. and Zeller R. (2004). Mouse limb deformity mutations disrupt a global control region within the large regulatory landscape required for Gremlin expression. Genes Dev.18, 1553-1564.

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• Michos O., Panman L., Vintersten K., Beier K., Zeller R. and Zuniga A. (2004). Gremlin mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131, 3401-3410.

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• Sturm, J., Keese, M., Zhang, H., Bönninghoff, R., Magdeburg, R., Vajkoczy, P., Post, S., Dono, R., Zeller, R. and Gretz, N. (2004). Liver regeneration in FGF-2-deficient mice: VEGF acts as potential functional substitute for FGF-2. Liver Int. 24, 161-168. 

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• Galli A., Roure A., Zeller R. and Dono R. (2003). Glypican-4 modulates FGF signalling and regulates dorso-ventral forebrain patterning in Xenopus embryos. Development 30, 4919-4929. 

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• Deller T., Korte M., Chabanis S., Drakew A., Schwegler H., Good-Stefani G., Zuniga A., Schwarz K., Bonhoeffer T., Zeller R*., Frotscher M.* and Mundel P.* (2003). Synaptopodin-deficient mice lack a spine apparatus and show deficits in synaptic plasticity. (*joint senior authors). Proc. Natl Acad Sci USA 100,10494-10499. 

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• Neuhaus P., Oustanina S., Loch T., Krüger M, Bober E., Dono R., Zeller R. and Braun T. (2003). Reduced mobility of FGF-mutant myoblasts might contribute to dystrophic changes in the musculature of FGF2/FGF6/mdx triple mouse mutants. Mol. Cell. Biol. 23, 6037-6048. 

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