The pathogenic mechanism of syndactyly type V identified in a Hoxd13Q50R knock-in mice
- Han Wang1,2, Xiumin Chen1, Xiaolu Meng1, Yixuan Cao1, Shirui Han1, Keqiang Liu1, Ximeng Zhao1, Xiuli Zhao1, Xue Zhang1
Author information
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1McKusick-Zhang Center for Genetic Medicine, State Key Laboratory of Complex Severe and Rare Diseases, Department of Medical Genetics, Institute of Basic Medical Sciences Chinese Academy of Medical Sciences, School of Basic Medicine Peking Union Medical College, Beijing 100005, China;
2Department of Orthopedics, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing 100730, China
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Received |
Revised |
Published |
24 Apr 2023 |
30 Jan 2024 |
10 Jul 2024 |
Issue Date |
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10 Jul 2024 |
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References
1. Malik S.Syndactyly: phenotypes, genetics and current classification. Eur. J. Hum. Genet. 20, 817-824 (2012).
2. Zhao, X.et al.Mutations in HOXD13 underlie syndactyly type V and a novel brachydactyly-syndactyly syndrome. Am. J. Hum. Genet. 80, 361-371 (2007).
3. Brison, N., Debeer, P.& Tylzanowski, P. Joining the fingers: a HOXD13 story. Dev. Dyn. 243, 37-48 (2014).
4. Malik S.& Grzeschik, K. H. Synpolydactyly: clinical and molecular advances. Clin. Genet. 73, 113-120 (2008).
5. Caronia, G.et al. An I47L substitution in the HOXD13 homeodomain causes a novel human limb malformation by producing a selective loss of function. Development 130, 1701-1712 (2003).
6. Saunders J. W.Jr. The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J. Exp. Zool. 108, 363-403 (1948).
7. Ogura, T.et al. Evidence that Shh cooperates with a retinoic acid-inducible cofactor to establish ZPA-like activity. Development 122, 537-542 (1996).
8. Tickle C.& Towers, M. Sonic Hedgehog signaling in limb development. Front. Cell Dev. Biol. 5, 14(2017).
9. Young J. J.& Tabin, C. J. Saunders's framework for understanding limb development as a platform for investigating limb evolution. Dev. Biol. 429, 401-408 (2017).
10. Lopez-Rios, J. The many lives of SHH in limb development and evolution. Semin. Cell Dev. Biol. 49, 116-124 (2016).
11. Galli, A.et al.Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. PLoS Genet. 6, e1000901(2010).
12. Niswander, L. & Martin, G. R. FGF-4 and BMP-2 have opposite effects on limb growth. Nature 361, 68-71 (1993).
13. Sun, X., Martin, G. R.& Lewandoski, M. Fgf8 signalling from the AER is essential for normal limb development. Nat. Genet. 26, 460-463 (2000).
14. Rodrigues, A. R.et al. Integration of Shh and Fgf signaling in controlling Hox gene expression in cultured limb cells. Proc. Natl. Acad. Sci. USA 114, 3139-3144 (2017).
15. Pajni-Underwood, S.et al. BMP signals control limb bud interdigital programmed cell death by regulating FGF signaling. Development 134, 2359-2368 (2007).
16. Hernández-Martínez, R. & Covarrubias, L. Interdigital cell death function and regulation: new insights on an old programmed cell death model. Dev. Growth Differ. 53, 245-258 (2011).
17. Benazet, J. D.et al. A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Science 323, 1050-1053 (2009).
18. Lancman, J. J.et al.Downregulation of Grem1 expression in the distal limb mesoderm is a necessary precondition for phalanx development. Dev. Dyn. 251, 1439-1455 (2022).
19. Sommer, D.et al.TALEN-mediated genome engineering to generate targeted mice. Chromosome Res. 23, 43-55 (2015).
20. Ceccaldi, R., Rondinelli, B.& D'Andrea, A. D. Repair pathway choices and consequences at the double-strand break. Trends Cell Biol. 26, 52-64 (2016).
21. Li, T.et al.TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res. 39, 359-372 (2011).
22. Haramis, A. G., Brown, J. M. & Zeller, R. The limb deformity mutation disrupts the SHH/FGF-4 feedback loop and regulation of 5' HoxD genes during limb pattern formation. Development 121, 4237-4245 (1995).
23. Zuzarte-Luis, V. & Hurle, J. M. Programmed cell death in the developing limb. Int. J. Dev. Biol. 46, 871-876 (2002).
24. Wrighton, K. H., Lin, X.& Feng, X. H. Phospho-control of TGF-beta superfamily signaling. Cell Res. 19, 8-20 (2009).
25. Ahn, S. & Joyner, A. L. Dynamic changes in the response of cells to positive Hedgehog signaling during mouse limb patterning. Cell 118, 505-516 (2004).
26. Sheth, R.et al. Decoupling the function of Hox and Shh in developing limb reveals multiple inputs of Hox genes on limb growth. Development 140, 2130-2138 (2013).
27. Takatalo, M.et al.Expression of the novel Golgi protein GoPro49 is developmentally regulated during mesenchymal differentiation. Dev. Dyn. 237, 2243-2255 (2008).
28. Ye, J.et al.MicroRNA6715p inhibits cell proliferation, migration and invasion in nonsmall cell lung cancer by targeting MFAP3L. Mol. Med. Rep. 25, 30(2022).
29. Krumlauf, R. Hox genes in vertebrate development. Cell 78, 191-201 (1994).
30. Mallo M.Reassessing the role of hox genes during vertebrate development and evolution. Trends Genet. 34, 209-217 (2018).
31. Salsi, V.et al.Hoxd13 binds in vivo and regulates the expression of genes acting in key pathways for early limb and skeletal patterning. Dev. Biol. 317, 497-507 (2008).
32. Delgado I.& Torres, M. Coordination of limb development by crosstalk among axial patterning pathways. Dev. Biol. 429, 382-386 (2017).
33. Kmita, M.et al. Early developmental arrest of mammalian limbs lacking HoxA/ HoxD gene function. Nature 435, 1113-1116 (2005).
34. Villavicencio-Lorini, P. et al. Homeobox genes d11-d13 and a13 control mouse autopod cortical bone and joint formation. J. Clin. Investig. 120, 1994-2004 (2010).
35. Ibrahim, D. M.et al. A homozygous HOXD13 missense mutation causes a severe form of synpolydactyly with metacarpal to carpal transformation. Am. J. Med. Genet. A 170, 615-621 (2016).
36. Martin P.Tissue patterning in the developing mouse limb. Int. J. Dev. Biol. 34, 323-336 (1990).
37. Yokouchi, Y.et al. BMP-2/-4 mediates programmed cell death in chicken limb buds. Development 122, 3725-3734 (1996).
38. Badugu, A.et al.Digit patterning during limb development as a result of the BMP-receptor interaction. Sci. Rep. 2, 991(2012).
39. Montavon T.& Soshnikova, N. Hox gene regulation and timing in embryogenesis. Semin. Cell Dev. Biol. 34, 76-84 (2014).
40. Chiang, C.et al. Cyclopia and defective axial patterning in mice lacking Sonic Hedgehog gene function. Nature 383, 407-413 (1996).
41. Pizard, A., Haramis, A.& Carrasco, A. E. Whole‐mount in situ hybridization and detection of RNAs in vertebrate embryos and isolated organs. Curr. Protoc. Mol. Biol. Ch. 14(2004).
42. Chitramuthu B. P.& Bennett, H. P. High-resolution whole mount in situ hybridization within zebrafish embryos to study gene expression and function. J. Vis. Exp. e50644(2013).
Funding
Xiuli Zhao (xiulizhao@ibms.pumc.edu.cn) or Xue Zhang (xuezhang@pumc.edu.cn)