دورية أكاديمية
Suppression of apoptosis impairs phalangeal joint formation in the pathogenesis of brachydactyly type A1.
العنوان: | Suppression of apoptosis impairs phalangeal joint formation in the pathogenesis of brachydactyly type A1. |
---|---|
المؤلفون: | Leung AOW; School of Biomedical Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China., Poon ACH; School of Biomedical Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China., Wang X; School of Biomedical Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China., Feng C; School of Biomedical Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China.; Hebei Orthopedic Clinical Research Center, The Third Hospital of Hebei Medical University, 050051, Shijiazhuang, Hebei, China., Chen P; School of Biomedical Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China.; Department of Orthopaedics Surgery and Traumatology, The University of Hong Kong -Shenzhen Hospital (HKU-SZH), Shenzhen, China., Zheng Z; School of Biomedical Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China., To MK; Department of Orthopaedics Surgery and Traumatology, The University of Hong Kong -Shenzhen Hospital (HKU-SZH), Shenzhen, China.; Department of Orthopaedics and Traumatology, The University of Hong Kong, Pokfulam, Hong Kong, China., Chan WCW; School of Biomedical Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China. cwilson@hku.hk.; Department of Orthopaedics Surgery and Traumatology, The University of Hong Kong -Shenzhen Hospital (HKU-SZH), Shenzhen, China. cwilson@hku.hk., Cheung M; School of Biomedical Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China., Chan D; School of Biomedical Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China. chand@hku.hk. |
المصدر: | Nature communications [Nat Commun] 2024 Mar 12; Vol. 15 (1), pp. 2229. Date of Electronic Publication: 2024 Mar 12. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101528555 Publication Model: Electronic Cited Medium: Internet ISSN: 2041-1723 (Electronic) Linking ISSN: 20411723 NLM ISO Abbreviation: Nat Commun Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: [London] : Nature Pub. Group |
مواضيع طبية MeSH: | Hedgehog Proteins*/metabolism , Brachydactyly*/genetics , Brachydactyly*/metabolism, Mice ; Animals ; Joints/metabolism ; Apoptosis |
مستخلص: | Apoptosis occurs during development when a separation of tissues is needed. Synovial joint formation is initiated at the presumptive site (interzone) within a cartilage anlagen, with changes in cellular differentiation leading to cavitation and tissue separation. Apoptosis has been detected in phalangeal joints during development, but its role and regulation have not been defined. Here, we use a mouse model of brachydactyly type A1 (BDA1) with an Ihh E95K mutation, to show that a missing middle phalangeal bone is due to the failure of the developing joint to cavitate, associated with reduced apoptosis, and a joint is not formed. We showed an intricate relationship between IHH and interacting partners, CDON and GAS1, in the interzone that regulates apoptosis. We propose a model in which CDON/GAS1 may act as dependence receptors in this context. Normally, the IHH level is low at the center of the interzone, enabling the "ligand-free" CDON/GAS1 to activate cell death for cavitation. In BDA1, a high concentration of IHH suppresses apoptosis. Our findings provided new insights into the role of IHH and CDON in joint formation, with relevance to hedgehog signaling in developmental biology and diseases. (© 2024. The Author(s).) |
References: | Sanz-Ezquerro, J. J. & Tickle, C. Digital development and morphogenesis. J. Anat. 202, 51–58 (2003). (PMID: 12587920157106310.1046/j.1469-7580.2003.00134.x) Craig, F. M., Bentley, G. & Archer, C. W. The spatial and temporal pattern of collagens I and II and keratan sulphate in the developing chick metatarsophalangeal joint. Development 99, 383–391 (1987). (PMID: 295826610.1242/dev.99.3.383) Storm, E. E. et al. Limb alterations in brachypodism mice due to mutations in a new member of the TGF beta-superfamily. Nature 368, 639–643 (1994). (PMID: 814585010.1038/368639a0) Storm, E. E. & Kingsley, D. M. GDF5 coordinates bone and joint formation during digit development. Dev. Biol. 209, 11–27 (1999). (PMID: 1020873910.1006/dbio.1999.9241) Hartmann, C. & Tabin, C. J. Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton. Cell 104, 341–351 (2001). (PMID: 1123939210.1016/S0092-8674(01)00222-7) Guo, X. et al. Wnt/beta-catenin signaling is sufficient and necessary for synovial joint formation. Genes Dev. 18, 2404–2417 (2004). (PMID: 1537132752299010.1101/gad.1230704) Später, D., Hill, T. P., Gruber, M. & Hartmann, C. Role of canonical Wnt-signalling in joint formation. Eur. Cell Mater. 12, 71–80 (2006). (PMID: 1711537610.22203/eCM.v012a09) Später, D. et al. Wnt9a signaling is required for joint integrity and regulation of Ihh during chondrogenesis. Development 133, 3039–3049 (2006). (PMID: 1681844510.1242/dev.02471) Lovinescu, I., Koyama, E. & Pacifici, M. Roles of FGF-10 on the development of diathrodial limb joints. Penn. Dent. J. (Philos.) 103, 9 (2003). Mak, K. K., Chen, M. H., Day, T. F., Chuang, P. T. & Yang, Y. Wnt/beta-catenin signaling interacts differentially with Ihh signaling in controlling endochondral bone and synovial joint formation. Development 133, 3695–3707 (2006). (PMID: 1693607310.1242/dev.02546) Koyama, E. et al. Synovial joint formation during mouse limb skeletogenesis: roles of Indian hedgehog signaling. Ann. N. Y Acad. Sci. 1116, 100–112 (2007). (PMID: 18083924267354510.1196/annals.1402.063) Baldridge, D., Shchelochkov, O., Kelley, B. & Lee, B. Signaling pathways in human skeletal dysplasias. Annu. Rev. Genomics Hum. Genet. 11, 189–217 (2010). (PMID: 2069081910.1146/annurev-genom-082908-150158) Chang, S. C. et al. Cartilage-derived morphogenetic proteins. New members of the transforming growth factor-beta superfamily predominantly expressed in long bones during human embryonic development. J. Biol. Chem. 269, 28227–28234 (1994). (PMID: 796176110.1016/S0021-9258(18)46918-9) Francis-West, P. H., Parish, J., Lee, K. & Archer, C. W. BMP/GDF-signalling interactions during synovial joint development. Cell Tissue Res. 296, 111–119 (1999). (PMID: 1019997110.1007/s004410051272) Feng, C. et al. Lgr5 and Col22a1 mark progenitor cells in the lineage toward juvenile articular chondrocytes. Stem Cell Rep. 13, 713–729 (2019). (PMID: 10.1016/j.stemcr.2019.08.006) Kozhemyakina, E. et al. Identification of a Prg4-expressing articular cartilage progenitor cell population in mice. Arthritis Rheumatol. 67, 1261–1273 (2015). (PMID: 25603997441482310.1002/art.39030) Mundlos, S. The brachydactylies: a molecular disease family. Clin. Genet. 76, 123–136 (2009). (PMID: 1979028910.1111/j.1399-0004.2009.01238.x) Niedermaier, M. et al. An inversion involving the mouse Shh locus results in brachydactyly through dysregulation of Shh expression. J. Clin. Invest. 115, 900–909 (2005). (PMID: 15841179107042010.1172/JCI200523675) Seemann, P. et al. Activating and deactivating mutations in the receptor interaction site of GDF5 cause symphalangism or brachydactyly type A2. J. Clin. Invest. 115, 2373–2381 (2005). (PMID: 16127465119037410.1172/JCI25118) Lehmann, K. et al. A novel R486Q mutation in BMPR1B resulting in either a brachydactyly type C/symphalangism-like phenotype or brachydactyly type A2. Eur. J. Hum. Genet. 14, 1248–1254 (2006). (PMID: 1695768210.1038/sj.ejhg.5201708) Gao, B. et al. A mutation in Ihh that causes digit abnormalities alters its signalling capacity and range. Nature 458, 1196 (2009). (PMID: 1925247910.1038/nature07862) Witte, F., Chan, D., Economides, A. N., Mundlos, S. & Stricker, S. Receptor tyrosine kinase-like orphan receptor 2 (ROR2) and Indian hedgehog regulate digit outgrowth mediated by the phalanx-forming region. Proc. Natl Acad. Sci. USA 107, 14211–14216 (2010). (PMID: 20660756292254410.1073/pnas.1009314107) Liu, M. et al. A novel heterozygous mutation in the Indian hedgehog gene (IHH) is associated with brachydactyly type A1 in a Chinese family. J. Hum. Genet. 51, 727–731 (2006). (PMID: 1687136410.1007/s10038-006-0012-6) Byrnes, A. M. et al. Brachydactyly A-1 mutations restricted to the central region of the N-terminal active fragment of Indian Hedgehog. Eur. J. Hum. Genet. 17, 1112–1120 (2009). (PMID: 19277064298660210.1038/ejhg.2009.18) Knosp, W. M., Scott, V., Bächinger, H. P. & Stadler, H. S. HOXA13 regulates the expression of bone morphogenetic proteins 2 and 7 to control distal limb morphogenesis. Development 131, 4581–4592 (2004). (PMID: 1534248210.1242/dev.01327) McCready, M. E. et al. A novel mutation in the IHH gene causes brachydactyly type A1: a 95-year-old mystery resolved. Hum. Genet. 111, 368–375 (2002). (PMID: 1238477810.1007/s00439-002-0815-2) Guo, S. et al. Missense mutations in IHH impair Indian Hedgehog signaling in C3H10T1/2 cells: implications for brachydactyly type A1, and new targets for Hedgehog signaling. Cell Mol. Biol. Lett. 15, 153–176 (2010). (PMID: 2002469210.2478/s11658-009-0040-2) Ma, G. et al. Indian hedgehog mutations causing brachydactyly type A1 impair Hedgehog signal transduction at multiple levels. Cell Res. 21, 1343–1357 (2011). (PMID: 21537345319347110.1038/cr.2011.76) Duprez, D. et al. Overexpression of BMP-2 and BMP-4 alters the size and shape of developing skeletal elements in the chick limb. Mech. Dev. 57, 145–157 (1996). (PMID: 884339210.1016/0925-4773(96)00540-0) Zou, H., Wieser, R., Massagué, J. & Niswander, L. Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 11, 2191–2203 (1997). (PMID: 930353527539110.1101/gad.11.17.2191) Brunet, L. J., McMahon, J. A., McMahon, A. P. & Harland, R. M. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 280, 1455–1457 (1998). (PMID: 960373810.1126/science.280.5368.1455) Tsumaki, N. et al. Role of CDMP-1 in skeletal morphogenesis: promotion of mesenchymal cell recruitment and chondrocyte differentiation. J. Cell Biol. 144, 161–173 (1999). (PMID: 9885252214812510.1083/jcb.144.1.161) Mitrovic, D. R. Development of the metatarsophalangeal joint of the chick embryo: morphological, ultrastructural and histochemical studies. Am. J. Anat. 150, 333–347 (1977). (PMID: 92063310.1002/aja.1001500207) Mori, C. et al. Programmed cell death in the interdigital tissue of the fetal mouse limb is apoptosis with DNA fragmentation. Anat. Rec. 242, 103–110 (1995). (PMID: 760497310.1002/ar.1092420114) Archer, C. W., Dowthwaite, G. P. & Francis‐West, P. Development of synovial joints. Birth Defects Res. C Embryo Today 69, 144–155 (2003). (PMID: 1295585810.1002/bdrc.10015) Fernández-Terán, M. A., Hinchliffe, J. R. & Ros, M. A. Birth and death of cells in limb development: a mapping study. Dev. Dyn. 235, 2521–2537 (2006). (PMID: 1688106310.1002/dvdy.20916) Spagnoli, A. et al. TGF-beta signaling is essential for joint morphogenesis. J. Cell Biol. 177, 1105–1117 (2007). (PMID: 17576802206436910.1083/jcb.200611031) Provot, S. et al. Hif-1alpha regulates differentiation of limb bud mesenchyme and joint development. J. Cell Biol. 177, 451–464 (2007). (PMID: 17470636206482810.1083/jcb.200612023) Ito, M. M. & Kida, M. Y. Morphological and biochemical re-evaluation of the process of cavitation in the rat knee joint: cellular and cell strata alterations in the interzone. J. Anat. 197, 659–679 (2000). (PMID: 11197539146818110.1046/j.1469-7580.2000.19740659.x) Kavanagh, E., Abiri, M., Bland, Y. S. & Ashhurst, D. E. Division and death of cells in developing synovial joints and long bones. Cell Biol. Int. 26, 679–688 (2002). (PMID: 1217567110.1006/cbir.2002.0918) Chung, U. I., Schipani, E., McMahon, A. P. & Kronenberg, H. M. Indian hedgehog couples chondrogenesis to osteogenesis in endochondral bone development. J. Clin. Invest. 107, 295–304 (2001). (PMID: 1116015319919910.1172/JCI11706) Adams, S. L., Cohen, A. J. & Lassová, L. Integration of signaling pathways regulating chondrocyte differentiation during endochondral bone formation. J. Cell Physiol. 213, 635–641 (2007). (PMID: 1788625610.1002/jcp.21262) Koyama, E. et al. Conditional Kif3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis. Development 134, 2159–2169 (2007). (PMID: 1750741610.1242/dev.001586) Briscoe, J. & Thérond, P. P. The mechanisms of Hedgehog signalling and its roles in development and disease. Nat. Rev. Mol. Cell Biol. 14, 416–429 (2013). (PMID: 2371953610.1038/nrm3598) Allen, B. L. et al. Overlapping roles and collective requirement for the coreceptors GAS1, CDO, and BOC in SHH pathway function. Dev. Cell 20, 775–787 (2011). (PMID: 21664576312110410.1016/j.devcel.2011.04.018) Izzi, L. et al. Boc and Gas1 each form distinct Shh receptor complexes with Ptch1 and are required for Shh-mediated cell proliferation. Dev. Cell 20, 788–801 (2011). (PMID: 21664577343291310.1016/j.devcel.2011.04.017) Thibert, C. et al. Inhibition of neuroepithelial patched-induced apoptosis by sonic hedgehog. Science 301, 843–846 (2003). (PMID: 1290780510.1126/science.1085405) Mille, F. et al. The Patched dependence receptor triggers apoptosis through a DRAL-caspase-9 complex. Nat. Cell Biol. 11, 739–746 (2009). (PMID: 19465923284440710.1038/ncb1880) Delloye-Bourgeois, C. et al. Sonic Hedgehog promotes tumor cell survival by inhibiting CDON pro-apoptotic activity. PLoS Biol. 11, e1001623 (2013). (PMID: 23940460373545710.1371/journal.pbio.1001623) Delloye-Bourgeois, C., Rama, N., Brito, J., Le Douarin, N. & Mehlen, P. Sonic Hedgehog promotes the survival of neural crest cells by limiting apoptosis induced by the dependence receptor CDON during branchial arch development. Biochem. Biophys. Res. Commun. 452, 655–660 (2014). (PMID: 2519369710.1016/j.bbrc.2014.08.134) Gibert, B. et al. Regulation by miR181 family of the dependence receptor CDON tumor suppressive activity in neuroblastoma. J. Natl Cancer Inst. 106, dju318 (2014). (PMID: 2531324610.1093/jnci/dju318) Fombonne, J. et al. Patched dependence receptor triggers apoptosis through ubiquitination of caspase-9. Proc. Natl Acad. Sci. USA 109, 10510–10515 (2012). (PMID: 22679284338705610.1073/pnas.1200094109) Martinelli, D. C. & Fan, C. M. Gas1 extends the range of Hedgehog action by facilitating its signaling. Genes Dev. 21, 1231–1243 (2007). (PMID: 17504940186549410.1101/gad.1546307) Cabrera, J. R. et al. Gas1 is related to the glial cell-derived neurotrophic factor family receptors alpha and regulates Ret signaling. J. Biol. Chem. 281, 14330–14339 (2006). (PMID: 1655163910.1074/jbc.M509572200) Zarco, N., Gonzalez-Ramirez, R., Gonzalez, R. O. & Segovia, J. GAS1 induces cell death through an intrinsic apoptotic pathway. Apoptosis 17, 627–635 (2012). (PMID: 2231147010.1007/s10495-011-0696-8) Gao, B. et al. Mutations in IHH, encoding Indian hedgehog, cause brachydactyly type A-1. Nat. Genet 28, 386–388 (2001). (PMID: 1145538910.1038/ng577) Hellemans, J. et al. Homozygous mutations in IHH cause acrocapitofemoral dysplasia, an autosomal recessive disorder with cone-shaped epiphyses in hands and hips. Am. J. Hum. Genet. 72, 1040–1046 (2003). (PMID: 12632327118033510.1086/374318) Fitch, N. Classification and identification of inherited brachydactylies. J. Med. Genet. 16, 36–44 (1979). (PMID: 469884101277810.1136/jmg.16.1.36) Mortier, G. R., Kramer, P. P., Giedion, A. & Beemer, F. A. Acrocapitofemoral dysplasia: an autosomal recessive skeletal dysplasia with cone shaped epiphyses in the hands and hips. J. Med. Genet. 40, 201–207 (2003). (PMID: 12624140173538610.1136/jmg.40.3.201) McLellan, J. S. et al. The mode of Hedgehog binding to Ihog homologues is not conserved across different phyla. Nature 455, 979–983 (2008). (PMID: 18794898267968010.1038/nature07358) Bosanac, I. et al. The structure of SHH in complex with HHIP reveals a recognition role for the Shh pseudo active site in signaling. Nat. Struct. Mol. Biol. 16, 691–697 (2009). (PMID: 1956160910.1038/nsmb.1632) Kavran, J. M., Ward, M. D., Oladosu, O. O., Mulepati, S. & Leahy, D. J. All mammalian Hedgehog proteins interact with cell adhesion molecule, down-regulated by oncogenes (CDO) and brother of CDO (BOC) in a conserved manner. J. Biol. Chem. 285, 24584–24590 (2010). (PMID: 20519495291569410.1074/jbc.M110.131680) Chamberlain, C. E., Jeong, J., Guo, C., Allen, B. L. & McMahon, A. P. Notochord-derived Shh concentrates in close association with the apically positioned basal body in neural target cells and forms a dynamic gradient during neural patterning. Development 135, 1097–1106 (2008). (PMID: 1827259310.1242/dev.013086) Raz, R. et al. The mutation ROR2W749X, linked to human BDB, is a recessive mutation in the mouse, causing brachydactyly, mediating patterning of joints and modeling recessive Robinow syndrome. Development 135, 1713–1723 (2008). (PMID: 1835386210.1242/dev.015149) Wang, B., Fallon, J. F. & Beachy, P. A. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100, 423–434 (2000). (PMID: 1069375910.1016/S0092-8674(00)80678-9) Litingtung, Y., Dahn, R. D., Li, Y., Fallon, J. F. & Chiang, C. Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 418, 979–983 (2002). (PMID: 1219854710.1038/nature01033) Tenzen, T. et al. The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev. Cell 10, 647–656 (2006). (PMID: 1664730410.1016/j.devcel.2006.04.004) Zhang, W., Kang, J. S., Cole, F., Yi, M. J. & Krauss, R. S. Cdo functions at multiple points in the Sonic Hedgehog pathway, and Cdo-deficient mice accurately model human holoprosencephaly. Dev. Cell 10, 657–665 (2006). (PMID: 1664730310.1016/j.devcel.2006.04.005) Tian, H. et al. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478, 255–259 (2011). (PMID: 21927002425196710.1038/nature10408) Placzek, M. & Briscoe, J. Sonic hedgehog in vertebrate neural tube development. Int. J. Dev. Biol. 62, 225–234 (2018). (PMID: 2961673110.1387/ijdb.170293jb) Echevarría-Andino, M. L. & Allen, B. L. The hedgehog co-receptor BOC differentially regulates SHH signaling during craniofacial development. Development 147, dev189076 (2020). (PMID: 33060130775863510.1242/dev.189076) Rabadán, M. A., Usieto, S., Lavarino, C. & Martí, E. Identification of a putative transcriptome signature common to neuroblastoma and neural crest cells. Dev. Neurobiol. 73, 815–827 (2013). (PMID: 2377618510.1002/dneu.22099) Lee, C. S. & Fan, C. M. Embryonic expression patterns of the mouse and chick Gas1 genes. Mech. Dev. 101, 293–297 (2001). (PMID: 1123109410.1016/S0925-4773(01)00283-0) Dominguez-Monzon, G., Benitez, J. A., Vergara, P., Lorenzana, R. & Segovia, J. Gas1 inhibits cell proliferation and induces apoptosis of human primary gliomas in the absence of Shh. Int. J. Dev. Neurosci. 27, 305–313 (2009). (PMID: 1946062410.1016/j.ijdevneu.2009.03.009) Shwartz, Y., Viukov, S., Krief, S. & Zelzer, E. Joint development involves a continuous influx of Gdf5-positive cells. Cell Rep. 15, 2577–2587 (2016). (PMID: 27292641492097610.1016/j.celrep.2016.05.055) Beachy, P. A., Hymowitz, S. G., Lazarus, R. A., Leahy, D. J. & Siebold, C. Interactions between Hedgehog proteins and their binding partners come into view. Genes Dev. 24, 2001–2012 (2010). (PMID: 20844013293936210.1101/gad.1951710) Fuse, N. et al. Sonic hedgehog protein signals not as a hydrolytic enzyme but as an apparent ligand for patched. Proc. Natl Acad. Sci. USA 96, 10992–10999 (1999). (PMID: 105001133423110.1073/pnas.96.20.10992) Craig, F. M., Bayliss, M. T., Bentley, G. & Archer, C. W. A role for hyaluronan in joint development. J. Anat. 171, 17–23 (1990). (PMID: 17070451257124) Pitsillides, A. A., Archer, C. W., Prehm, P., Bayliss, M. T. & Edwards, J. C. Alterations in hyaluronan synthesis during developing joint cavitation. J. Histochem. Cytochem. 43, 263–273 (1995). (PMID: 786885610.1177/43.3.7868856) Matsumoto, K. et al. Conditional inactivation of Has2 reveals a crucial role for hyaluronan in skeletal growth, patterning, chondrocyte maturation and joint formation in the developing limb. Development 136, 2825–2835 (2009). (PMID: 19633173273040910.1242/dev.038505) Liu, J. et al. Sonic hedgehog signaling directly targets Hyaluronic Acid Synthase 2, an essential regulator of phalangeal joint patterning. Dev. Biol. 375, 160–171 (2013). (PMID: 2331312510.1016/j.ydbio.2012.12.018) Toole, B. P. Hyaluronan in morphogenesis. J. Intern. Med. 242, 35–40 (1997). (PMID: 926056410.1046/j.1365-2796.1997.00171.x) McKallip, R. J. et al. Role of CD44 in activation-induced cell death: CD44-deficient mice exhibit enhanced T cell response to conventional and superantigens. Int. Immunol. 14, 1015–1026 (2002). (PMID: 1220239910.1093/intimm/dxf068) Matsuda, S., Mishima, K., Yoshimura, Y., Hatta, T. & Otani, H. Apoptosis in the development of the temporomandibular joint. Anat. Embryol. (Berl.) 196, 383–391 (1997). (PMID: 940684010.1007/s004290050106) Amin, S., Matalova, E., Simpson, C., Yoshida, H. & Tucker, A. S. Incudomalleal joint formation: the roles of apoptosis, migration and downregulation. BMC Dev. Biol. 7, 134 (2007). (PMID: 18053235222264110.1186/1471-213X-7-134) Gu, S. et al. BMPRIA mediated signaling is essential for temporomandibular joint development in mice. PLoS ONE 9, e101000 (2014). (PMID: 25093411412235210.1371/journal.pone.0101000) Abu-Hijleh, G., Reid, O. & Scothorne, R. J. Cell death in the developing chick knee joint: I. Spatial and temporal patterns. Clin. Anat. 10, 183–200 (1997). (PMID: 913588610.1002/(SICI)1098-2353(1997)10:3<183::AID-CA4>3.0.CO;2-V) Mitrovic, D. Development of the diarthrodial joints in the rat embryo. Am. J. Anat. 151, 475–485 (1978). (PMID: 64561310.1002/aja.1001510403) Negulescu, A. M. & Mehlen, P. Dependence receptors—the dark side awakens. FEBS J. 285, 3909–3924 (2018). (PMID: 2977600910.1111/febs.14507) Ruaro, M. E., Stebel, M., Vatta, P., Marzinotto, S. & Schneider, C. Analysis of the domain requirement in Gas1 growth suppressing activity. FEBS Lett. 481, 159–163 (2000). (PMID: 1099631610.1016/S0014-5793(00)02005-6) Stebel, M. et al. The growth suppressing gas1 product is a GPI-linked protein. FEBS Lett. 481, 152–158 (2000). (PMID: 1099631510.1016/S0014-5793(00)02004-4) Forcet, C. et al. The dependence receptor DCC (deleted in colorectal cancer) defines an alternative mechanism for caspase activation. Proc. Natl Acad. Sci. USA 98, 3416–3421 (2001). (PMID: 112480933066810.1073/pnas.051378298) Llambi, F. et al. The dependence receptor UNC5H2 mediates apoptosis through DAP-kinase. Embo J. 24, 1192–1201 (2005). (PMID: 1572935955639610.1038/sj.emboj.7600584) Hamburger, V. & Hamilton, H. L. A series of normal stages in the development of the chick embryo. Dev. Dyn. 195, 231–272 (1992). (PMID: 130482110.1002/aja.1001950404) Allen, B. L., Tenzen, T. & McMahon, A. P. The Hedgehog-binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev. 21, 1244–1257 (2007). (PMID: 17504941186549510.1101/gad.1543607) Edelheit, O., Hanukoglu, A. & Hanukoglu, I. Simple and efficient site-directed mutagenesis using two single-primer reactions in parallel to generate mutants for protein structure-function studies. BMC Biotechnol. 9, 61 (2009). (PMID: 19566935271194210.1186/1472-6750-9-61) Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. & Pease, L. R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51–59 (1989). (PMID: 274448710.1016/0378-1119(89)90358-2) Sasaki, H., Hui, C., Nakafuku, M. & Kondoh, H. A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124, 1313–1322 (1997). (PMID: 911880210.1242/dev.124.7.1313) Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003–1007 (2007). (PMID: 1793444910.1038/nature06196) Cole, F. & Krauss, R. S. Microform holoprosencephaly in mice that lack the Ig superfamily member Cdon. Curr. Biol. 13, 411–415 (2003). (PMID: 1262019010.1016/S0960-9822(03)00088-5) Sim, Y. J. et al. 2i Maintains a naive ground state in ESCs through two distinct epigenetic mechanisms. Stem Cell Rep. 8, 1312–1328 (2017). (PMID: 10.1016/j.stemcr.2017.04.001) Silva, J. et al. Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol. 6, e253 (2008). (PMID: 18942890257042410.1371/journal.pbio.0060253) Eakin, G. S. & Hadjantonakis, A. K. Production of chimeras by aggregation of embryonic stem cells with diploid or tetraploid mouse embryos. Nat. Protoc. 1, 1145–1153 (2006). (PMID: 17406396288316610.1038/nprot.2006.173) Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902.e1821 (2019). (PMID: 31178118668739810.1016/j.cell.2019.05.031) Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005). (PMID: 16199517123989610.1073/pnas.0506580102) |
المشرفين على المادة: | 0 (Hedgehog Proteins) |
SCR Disease Name: | Brachydactyly type A1 |
تواريخ الأحداث: | Date Created: 20240313 Date Completed: 20240314 Latest Revision: 20240316 |
رمز التحديث: | 20240316 |
مُعرف محوري في PubMed: | PMC10933404 |
DOI: | 10.1038/s41467-024-45053-0 |
PMID: | 38472182 |
قاعدة البيانات: | MEDLINE |
تدمد: | 2041-1723 |
---|---|
DOI: | 10.1038/s41467-024-45053-0 |