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Low-Density Lipoprotein Receptor-Related Protein-5 Binds to Axin and Regulates the Canonical Wnt Signaling Pathway
Open accessAbstract
To understand how the Wnt coreceptor LRP-5 is involved in transducing the canonical Wnt signals, we identified Axin as a protein that interacts with the intracellular domain of LRP-5. LRP-5, when expressed in fibroblast cells, showed no effect on the canonical Wnt signaling pathway by itself, but acted synergistically with Wnt. In contrast, LRP-5 mutants lacking the extracellular domain functioned as constitutively active forms that bind Axin and that induce LEF-1 activation by destabilizing Axin and stabilizing beta-catenin. Addition of Wnt caused the translocation of Axin to the membrane and enhanced the interaction between Axin and LRP-5. In addition, the LRP-5 sequences involved in interactions with Axin are required for LEF-1 activation. Thus, we conclude that the binding of Axin to LRP-5 is an important part of the Wnt signal transduction pathway.
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“The canonical Wnt signalling pathway is mainly involved in cell proliferation and survival in vital biological processes, including organogenesis and embryogenesis.1,2”
From Canonical Wnt pathway and the LDL receptor superfamily in neuronal cholesterol homeostasis and function (2024) · cites this paper as [1]
In the citing paper
“The binding of Wnt to the Fz/LRP5/6 complex induces the membrane translocation of a key negative regulator of signaling Axin, which binds to a conserved sequence in the cytoplasmic tail of LRP5/6.27,28”
From Wnt signal transduction pathways (2008) · cites this paper as [27]
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“A more definitive link has been documented (Mao et al., 2001) between a destruction complex protein, Axin (Hamada et al., 1999; Willert et al., 1999), and the cytosolic domain of a second type of Wg receptor, the LDL receptor-related protein (LRP) encoded by arr in the fly (Wehrli et al., 2000).”
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BackgroundInfluentialWnt Signaling: Role in Regulation of Haematopoiesis
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Wnt signalling induces accumulation of phosphorylated β-catenin in two distinct cytosolic complexes
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Theka, I., Sottile, F., Cammisa, M., Bonnin, S., Sánchez-Delgado, M., Vicino, U. D., Neguembor, M. V., Arumugam, K., Aulicino, F., Monk, D., et al. (2019) · Scientific Reports · doi:10.1038/s41598-018-37442-5 · Cited by 42
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Regulated proteolytic processing of LRP6 results in release of its intracellular domain
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“Moreover, the low-density lipoprotein receptor-related proteins (LRP) LRP-5/6 act as co-receptors specifically in the canonical pathway (Mao et al. 2001a,b, He et al. 2004), whereas some membrane-attached heparan sulfate proteoglycans, including glypicans and syndecans, play different modulatory…”
BackgroundDelayed dopaminergic neuron differentiation in Lrp6 mutant mice
Castelo‐Branco, G., Andersson, E. R., Minina, E., Sousa, K. M., Ribeiro, D., Kokubu, C., Imai, K., Prakash, N., Wurst, W., & Arenas, E. (2009) · Developmental Dynamics · doi:10.1002/dvdy.22094 · Cited by 39
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β-catenin mediates fluoride-induced aberrant osteoblasts activity and osteogenesis
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BackgroundInfluentialA novel role of LRP5 in tubulointerstitial fibrosis through activating TGF-β/Smad signaling
He, X., Cheng, R., Huang, C., Takahashi, Y., Yang, Y., Benyajati, S., Chen, Y., Zhang, X. A., & Ma, J. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-0142-x · Cited by 35
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The Ubiquitin System: a Regulatory Hub for Intellectual Disability and Autism Spectrum Disorder
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LRP5/6 in Wnt Signaling and Tumorigenesis
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“These receptors appear to transduce the Wnt/β-catenin signal by binding and recruiting Axin to the cell membrane [11].”
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“Initially considered as endocytic receptors involved in lipoprotein metabolism (Nykjaer and Willnow, 2002), recent studies have demonstrated that the LRPs interact with a variety of adaptor and scaffold proteins implicated in signaling of several signal transduction pathways including the Wnt pathway (Mao et al., 2001…”
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The Daam2–VHL–Nedd4 axis governs developmental and regenerative oligodendrocyte differentiationPreprint
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“A critical step during Wnt signal transduction is the clustering of Wnt receptor complexes into signalosomes (Mao et al. 2001; He et al. 2004; Bilic ́ et al. 2007; Schwarz-Romond et al. 2007; Pan et al. 2008; MacDonald et al. 2009; Qin et al. 2009).”
BackgroundInhibition of phosphodiesterase 5 reduces bone mass by suppression of canonical Wnt signaling
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Self-citationDestruction complex dynamics: Wnt/β-catenin signaling alters Axin-GSK3β interactions inin vivo
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Integrin αEβ7+ T cells direct intestinal stem cell fate decisions via adhesion signaling
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Self-citationFunctional Characterization of a Small-Molecule Inhibitor of the DKK1-LRP6 Interaction
Iozzi, S., Remelli, R., Lelli, B., Diamanti, D., Pileri, S., Bracci, L., Roncarati, R., Caricasole, A., & Bernocco, S. (2012) · ISRN Molecular Biology · doi:10.5402/2012/823875 · Cited by 34
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Fujimuro, M., & Hayward, S. D. (2004) · Journal of Molecular Medicine · doi:10.1007/s00109-003-0519-7 · Cited by 33
“LRP-5 and LRP-6 are LDL-receptor-related proteins that are essential coreceptors for Wnt signaling [51, 52, 53].”
BackgroundPovelones, M., Howes, R., Fish, M., & Nusse, R. (2005) · Genetics · doi:10.1534/genetics.105.045245 · Cited by 32
“On the cytoplasmic side, Arr recruits Axn to the membrane (Mao et al. 2001; Tolwinski et al. 2003; Tamai et al. 2004).”
BackgroundLRP5/canonical Wnt signalling and healing of ischemic myocardium
Borrell-Pages, M., Vilahur, G., Romero, J. C., Casaní, L., Bejar, M. T., & Badimon, L. (2016) · Basic Research in Cardiology · doi:10.1007/s00395-016-0585-y · Cited by 31
“Low-density lipoprotein receptor-related protein 5 (LRP5) is a single membrane protein of the LRP superfamily required for activation of the canonical Wnt/b-catenin signalling pathway [31, 51].”
BackgroundThe physiological role of Wnt pathway in normal development and cancer
Li, X., Ortiz, M. A., & Kotula, L. (2020) · Experimental Biology and Medicine · doi:10.1177/1535370220901683 · Cited by 32
“complex and the stabilization of b-catenin.(39) More recent studies showed that the phosphorylated tail of LRP5/6 directly blocks GSK3 activity to prevent b-catenin degradation.”
BackgroundZema, S., Pelullo, M., Nardozza, F., Felli, M. P., Screpanti, I., & Bellavia, D. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.613557 · Cited by 34
Davidson, G. R. (2021) · Handbook of experimental pharmacology · doi:10.1007/164_2021_526 · Cited by 35
The Wnt/β-catenin signalling pathway in Haematological Neoplasms
Yu, S., Han, R., & Gan, R. (2022) · Biomarker Research · doi:10.1186/s40364-022-00418-9 · Cited by 38
“Then, LRP5/6 can recruit the destruction complex and complete the phosphorylation of the other remaining groups [28], which initiates a positive feedback loop.”
BackgroundLrp4: A novel modulator of extracellular signaling in craniofacial organogenesis
Ohazama, A., Porntaveetus, T., Ota, M. S., Herz, J., & Sharpe, P. T. (2010) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.33372 · Cited by 33
“…of Wnt signaling, unlike Lrp5/6 which are Wnt co-activators, since increasing Lrp4 expression relative to Lrp5/ 6 suppresses Wnt signaling and because Lrp4 lacks an intracellular Axin binding domain [Pinson et al., 2000; Tamai et al., 2000; Herz, 2001; Mao et al., 2001; Weatherbee et al., 2006].”
BackgroundMissense Mutations in LRP5 Are Not a Common Cause of Idiopathic Osteoporosis in Adult Men
Crabbe, P., Balemans, W., Willaert, A., Pottelbergh, I. V., Cleiren, E., Coucke, P. J., Ai, M., Goemaere, S., Hul, W. V., Paepe, A. D., et al. (2005) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.050705 · Cited by 32
“The second YWTD-EGF domain of LRP5 most likely contains regions necessary for interaction with the Wnt-frizzled complex.((27)) Whereas no functional consequence on Wnt signal transduction was observed for the 4609G>A mutation, the IO phenotype observed in the patient carrying this mutation might be caused by other gen…”
BackgroundA blockade in Wnt signaling is activated following the differentiation of F9 teratocarcinoma cells
Shibamoto, S., Winer, J., Williams, M. P., & Polakis, P. G. (2003) · Experimental Cell Research · doi:10.1016/j.yexcr.2003.08.009 · Cited by 32
Otani, K., Dong, Y., Li, X., Lü, J., Zhang, N., Xu, L., Go, M. Y., Ng, E. K., Arakawa, T., Chan, F. K. L., et al. (2014) · The Journal of Pathology · doi:10.1002/path.4391 · Cited by 31
Βeta-catenin N-terminal domain: An enigmatic region prone to cancer causing mutations
Dar, M. S., Singh, P., Mir, R. A., & Dar, M. J. (2017) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2017.06.001 · Cited by 30
Kennell, J. A., & Cadigan, K. M. (2009) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-1145-2_1 · Cited by 31
Negative feedback regulation of Wnt signaling by Gβγ-mediated reduction of Dishevelled
Jung, H., Kim, H. J., Lee, S. K., Kim, R., Kopachik, W. J., Han, J., & Jho, E. (2009) · Experimental & Molecular Medicine · doi:10.3858/emm.2009.41.10.076 · Cited by 31
“In the presence of Wnt, Dishevelled and Axin (for canonical Wnt signaling) are translocated to membrane-bound Frizzled and LRP, respectively, and initiate downstream signaling (Mao et al., 2001; Tamai et al., 2004).”
p120-catenin in canonical Wnt signaling
Duñach, M., del Valle‐Pérez, B., & de Herreros, A. G. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1295920 · Cited by 31
“CK1c phosphorylates LRP5/6 in Thr1479 and maybe other residues creating docking sites for Axin, and enhancing the interaction of this protein with the LRP5/6 complex (Davidson et al., 2005; Mao et al., 2001) (Figure 1(F)).”
BackgroundLRP6 in mesenchymal stem cells is required for bone formation during bone growth and bone remodeling
Li, C., Williams, B. O., Cao, X., & Wan, M. (2014) · Bone Research · doi:10.1038/boneres.2014.6 · Cited by 30
Hojo, H., Ohba, S., Yano, F., & Chung, U. (2010) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-010-0199-7 · Cited by 33
Axin1 Prevents Salmonella Invasiveness and Inflammatory Response in Intestinal Epithelial Cells
Zhang, Y., Wu, S., Xia, Y., Chen, D., Petrof, E. O., Claud, E. C., Hsu, W., & Sun, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034942 · Cited by 30
“Axin1 has been shown to interact with many critical proteins, including b-catenin, GSK3 b, LRP5, and DVL1 [25,37,38,39].”
BackgroundCui, Y., Ma, W., Lei, F., Li, Q., Su, Y., Lin, X., Lin, C., Zhang, X., Ye, L., Wu, S., et al. (2016) · The Journal of Pathology · doi:10.1002/path.4725 · Cited by 30
The wnt/β-catenin signaling pathway participates in rhein ameliorating kidney injury in DN mice
Duan, S., Wu, Y., Zhao, C., Chen, M., Yuan, Y., Xing, C., & Zhang, B. (2015) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-015-2569-x · Cited by 29
Toggling a Conformational Switch in Wnt/β-catenin Signaling: Regulation of Axin Phosphorylation
Tacchelly-Benites, O., Wang, Z.-H., Yang, E., Lee, E., & Ahmed, Y. (2013) · Bioessays · doi:10.1002/bies.201300101 · Cited by 32
Axin phosphorylation in both Wnt-off and Wnt-on states requires the tumor suppressor APC
Tacchelly‐Benites, O., Wang, Z., Yang, E., Benchabane, H., Tian, A., Randall, M. P., & Ahmed, Y. F. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007178 · Cited by 29
Abuna, R. P. F., Oliveira, F. S., Adolpho, L. F., Fernandes, R. R., Rosa, A. L., & Beloti, M. M. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29674 · Cited by 29
“…cell lines, Lrp5‐deficient primary calvarial osteoblasts continually transmit signals independently of Lrp5, suggesting that other Wnt receptors, FZD and LRP6, are sufficient to activate the Wnt signaling pathway (Carron et al., 2003; Gong et al., 2001; Kato et al., 2002; Mao et al., 2001).”
BackgroundRegulation of hematopoiesis by activators and inhibitors of Wnt signaling from the niche
Schreck, C., Bock, F., Grziwok, S., Oostendorp, R. A. J., & Istvánffy, R. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12384 · Cited by 31
Dickkopf-1 in human oral cancer
Uzawa, K. (2011) · International Journal of Oncology · doi:10.3892/ijo.2011.1046 · Cited by 29
Discovering Implicit Entity Relation with the Gene-Citation-Gene Network
Song, M., Han, N. G., Kim, Y. H., Ding, Y., & Chambers, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0084639 · Cited by 29
Swain, R. K., Katoh, M., Medina, A., & Steinbeißer, H. (2005) · Cell Communication and Signaling · doi:10.1186/1478-811x-3-12 · Cited by 29
“This leads to the binding of axin to the cytoplasmic domain of LRP and its recruitment to the membrane [ 11 ].”
InfluentialExtracellular phosphorylation drives the formation of neuronal circuitry
Harada, H., Farhani, N., Wang, X.-F., Sugita, S., Charish, J., Attisano, L., Moran, M. F., Cloutier, J., Reber, M., Bremner, R., et al. (2019) · Nature Chemical Biology · doi:10.1038/s41589-019-0345-z · Cited by 29
Carbamazepine Enhances Adipogenesis by Inhibiting Wnt/β-Catenin Expression
Im, D. U., Kim, S. C., Chau, G. C., & Um, S. H. (2019) · Cells · doi:10.3390/cells8111460 · Cited by 30
“Expression levels of p-LRP6, p-GSK3β, β-catenin and active β-catenin were also reduced in cells overexpressing β-catenin after carbamazepine treatment (Figure 4C and Figure S2C).”
BackgroundInfluential
Metadata
- Authors
- Mao, J., Wang, J., Liu, B., Pan, W., Farr, G. H., Flynn, C., Yuan, H., Takada, S., Kimelman, D., Li, L., & Wu, D.
- Affiliations
- University of Connecticut (US)
- Chinese Academy of Sciences (CN)
- University of Washington (US)
- University of Rochester Medicine (US)
- Setsunan University (JP)
- Corresponding author
- Wu, Dianqing
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2001-04
- Volume
- 7
- Issue
- 4
- Pages
- 801-809
- ISSN
- 1097-2765 (ISSN-L)
- OpenAlex
- W2152769008
- Cited by
- 839
- References
- 32
- Citations by year
- 2026: 1 · 2025: 15 · 2024: 20 · 2023: 23 · 2022: 25 · 2021: 21 · 2020: 25 · 2019: 25 · 2018: 25 · 2017: 27 · 2016: 23 · 2015: 30 · 2014: 37 · 2013: 46 · 2012: 40
- FWCI
- 17.46
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r29gm053162-04)
- National Cancer Institute (R01CA085420, CA85420)
- National Institute of General Medical Sciences (GM53162, GM54167)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD027262, HD27262)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Signaling Pathways in Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Hedgehog Signaling Pathway Studies
- Keywords
- low-density lipoprotein receptor-related protein 5, Axin, Wnt/β-catenin signaling, β-catenin stabilization, protein-protein interaction
- MeSH terms
- Amino Acid Sequence, Animals, Mammals, Molecular Sequence Data, Protein Binding, Proteins, Proto-Oncogene Proteins, Receptors, LDL, Repressor Proteins, Signal Transduction, Gene Expression, Mutagenesis, 3T3 Cells, Protein Structure, Tertiary, Calcium-Calmodulin-Dependent Protein Kinases, COS Cells, LDL-Receptor Related Proteins, Zebrafish Proteins, Glycogen Synthase Kinase 3, Wnt Proteins, Mice, Axin Protein, Low Density Lipoprotein Receptor-Related Protein-5
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