Cited by 103Hedgehog Signaling Pathway StudiesGenetic and Kidney Cyst DiseasesDevelopmental Biology and Gene Regulation

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Tubby-like protein 3 (TULP3) regulates patterning in the mouse embryo through inhibition of Hedgehog signaling

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Norman, Ryan X., Ko, Hyuk W., Huang, Viola, Eun, Christine M., Abler, Lisa L., Zhang, Zhen, Sun, Xin, Eggenschwiler, Jonathan T.·2009·Human Molecular Genetics

DOI 10.1093/hmg/ddp113PMC PMC2671991

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Abstract

Tubby-like protein 3 (TULP3) is required for proper embryonic development in mice. Disruption of mouse Tulp3 results in morphological defects in the embryonic craniofacial regions, the spinal neural tube and the limbs. Here, we show that TULP3 functions as a novel negative regulator of Sonic hedgehog (Shh) signaling in the mouse. In Tulp3 mutants, ventral cell types in the lumbar neural tube, which acquire their identities in response to Shh signaling, are ectopically specified at the expense of dorsal cell types. Genetic epistasis experiments show that this ventralized phenotype occurs independently of Shh and the transmembrane protein Smoothened, but it is dependent on the transcription factor Gli2. The ventralized phenotype is also dependent on the kinesin II subunit Kif3A, which is required for intraflagellar transport and ciliogenesis. In addition, TULP3 is required for proper Shh-dependent limb patterning and for maintaining the correct balance between differentiation and proliferation in the neural tube. Finally, the localization of TULP3 to the tips of primary cilia raises the possibility that it regulates the Hedgehog pathway within this structure.

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A Laboratory manual
Ashburner, M. (1989) · Cold Spring Harbor Laboratory eBooks · Cited by 6,756
Manipulating the mouse embryo: A laboratory manual
Hogan, B. L. M., Costantini, F. D., & Lacy, E. (1986) · Cited by 4,460
Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function
Chiang, C. C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H., & Beachy, P. A. (1996) · Nature · doi:10.1038/383407a0 · Cited by 3,062
Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity
Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A., & McMahon, A. P. (1993) · Cell · doi:10.1016/0092-8674(93)90627-3 · Cited by 2,154
Manipulating the Mouse Embryo: A Laboratory Manual
Behringer, R. R., Gertsenstein, M., Nagy, K. V., & Nagy, A. (2002) · Cited by 2,046
Vertebrate Smoothened functions at the primary cilium
Corbit, K. C., Aanstad, P., Singla, V., Norman, A. R., Stainier, D. Y. R., & Reiter, J. F. (2005) · Nature · doi:10.1038/nature04117 · Cited by 1,481
Patched1 Regulates Hedgehog Signaling at the Primary Cilium
Rohatgi, R., Milenkovic, L., & Scott, M. P. (2007) · Science · doi:10.1126/science.1139740 · Cited by 1,426
Hedgehog signalling in the mouse requires intraflagellar transport proteins
Huangfu, D., Liu, A., Rakeman, A. S., Murcia, N. S., Niswander, L., & Anderson, K. V. (2003) · Nature · doi:10.1038/nature02061 · Cited by 1,425
A Core Complex of BBS Proteins Cooperates with the GTPase Rab8 to Promote Ciliary Membrane Biogenesis
Nachury, M. V., Loktev, A. V., Zhang, Q., Westlake, C. J., Peränen, J., Merdes, A., Slusarski, D. C., Scheller, R. H., Bazan, J. F., Sheffield, V. C., et al. (2007) · Cell · doi:10.1016/j.cell.2007.03.053 · Cited by 1,384
Hedgehog: functions and mechanisms
Varjosalo, M., & Taipale, J. (2008) · Genes & Development · doi:10.1101/gad.1693608 · Cited by 1,217

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Authors: Norman, R. X., Ko, H. W., Huang, V., Eun, C. M., Abler, L. L., Zhang, Z., Sun, X., & Eggenschwiler, J. T.
Affiliations: Princeton University (US)
University of Wisconsin–Madison (US)
Corresponding author: Eggenschwiler, Jonathan T.
ORCID: Ko, Hyuk W.
Huang, Viola
Abler, Lisa L.
Zhang, Zhen
Sun, Xin
Eggenschwiler, Jonathan T.
Venue: Human Molecular Genetics
Publisher: Oxford University Press (OUP)
Published: 2009-03-12
Volume: 18
Issue: 10
Pages: 1740-1754
ISSN: 0964-6906 (ISSN-L)
1460-2083
DOI: 10.1093/hmg/ddp113
PMC: PMC2671991
OpenAlex: W2170193319
Cited by: 103
References: 125
Citations by year: 2026: 3 · 2025: 6 · 2024: 9 · 2023: 5 · 2022: 6 · 2021: 7 · 2020: 10 · 2019: 6 · 2018: 5 · 2017: 5 · 2016: 7 · 2015: 5 · 2014: 4 · 2013: 4 · 2012: 9
FWCI: 2.82
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Human Molecular Genetics (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: New Jersey Commission on Spinal Cord Research
National Institutes of Health (IA 52242)
Directorate for Biological Sciences
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD045522, HD045522, HD050761, R01HD050761)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Hedgehog Signaling Pathway Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: TULP3, Sonic hedgehog signaling, Hedgehog signaling, neural tube patterning, GLI2, KIF3A, kinesin-2, intraflagellar transport, ciliogenesis, primary cilia, limb patterning, craniofacial defects, Smoothened, mouse embryo
MeSH terms: Animals, Embryo, Mammalian, Female, Humans, Male, Mice, Inbred C3H, Mice, Transgenic, Mutation, Proteins, Spinal Cord, Signal Transduction, Down-Regulation, Gene Expression Regulation, Developmental, Body Patterning, Intercellular Signaling Peptides and Proteins, Embryonic Development, Intracellular Signaling Peptides and Proteins, Mice, Hedgehog Proteins, Neural Tube

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Tubby-like protein 3 (TULP3) regulates patterning in the mouse embryo through inhibition of Hedgehog signaling

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