A unique stylopod patterning mechanism by shox2-controlled osteogenesis

Development (Cambridge)

Volumn 143, Issue 14, 2016, Pages 2548-2560

  Ye, Wenduo ^a   Song, Yingnan ^a,b   Huang, Zhen ^a,b   Osterwalder, Marco ^c   Ljubojevic, Anja ^d   Xu, Jue ^a,e   Bobick, Brent ^d   Abassah Oppong, Samuel ^d   Ruan, Ningsheng ^a,b   Shamby, Ross ^a   Yu, Diankun ^a   Zhang, Lu ^f   Cai, Chen Leng ^f   Visel, Axel ^c,g,h   Zhang, Yanding ^b   Cobb, John ^d   Chen, Yi Ping ^a,b  

^a Tulane University   (United States)

^b FUJIAN NORMAL UNIVERSITY   (China)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF CALGARY   (Canada)

^e SICHUAN UNIVERSITY   (China)

^f MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^g DOE JOINT GENOME INSTITUTE   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Limb; Patterning; Shox2; Skeleton; Stylopod

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MEIS; TRANSCRIPTION FACTOR PBX; TRANSCRIPTION FACTOR SHOX2; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; PROTEIN BINDING; SHOX2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR RUNX2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CELL FATE; CELL LINEAGE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; ENHANCER REGION; GENE; GENE CLUSTER; GENE EXPRESSION; GENE INACTIVATION; GENOME ANALYSIS; IMMUNOHISTOCHEMISTRY; LIMB DEVELOPMENT; MESENCHYME; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SHOX2 GENE; TRANSCRIPTION REGULATION; ANIMAL; BINDING SITE; BIOLOGICAL MODEL; CYTOLOGY; EMBRYOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; GENOME; LIMB; MESENCHYMAL STROMA CELL; METABOLISM; MORPHOGENESIS; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE;

ANIMALS; BASE SEQUENCE; BINDING SITES; BODY PATTERNING; CELL LINEAGE; CORE BINDING FACTOR ALPHA 1 SUBUNIT; ENHANCER ELEMENTS, GENETIC; EXTREMITIES; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HOMEODOMAIN PROTEINS; MESENCHYMAL STROMAL CELLS; MICE; MODELS, BIOLOGICAL; NUCLEOTIDE MOTIFS; OSTEOGENESIS; PROTEIN BINDING;

EID: 84978700538     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.138750     Document Type: Article

References (57)

1. Amin, S.,Donaldson, I. J.,Zannino, D. A.,Hensman, J.,Rattray, M.,Losa, M.,Spitz, F.,Ladam, F.,Sagerstrom, C. and Bobola, N. (2015). Hoxa2 selectively enhances Meis binding to change a branchial arch ground state. Dev. Cell 32, 265-277.
2. Attanasio, C.,Nord, A. S.,Zhu, Y.,Blow, M. J.,Biddie, S. C.,Mendenhall, E. M.,Dixon, J.,Wright, C.,Hosseini, R.,Akiyama, J. A. et al. (2014). Tissue-specific SMARCA4 binding at active and repressed regulatory elements during embryogenesis. Genome Res. 24, 920-929.
3. Barna, M.,Pandolfi, P. P. and Niswander, L. (2005). Gli3 and Plzf cooperate in proximal limb patterning at early stages of limb development. Nature 436, 277-281.
4. Bobick, B. E. and Cobb, J. (2012). Shox2 regulates progression through chondrogenesis in the mouse proximal limb. J. Cell Sci. 125, 6071-6083.
5. Capellini, T. D.,Zappavigna, V. and Selleri, L. (2011). Pbx homeodomain proteins: TALEnted regulators of limb patterning and outgrowth. Dev. Dyn. 240, 1063-1086.
6. Choe, S.-K.,Lu, P.,Nakamura, M.,Lee, J. and Sagerstrom, C. G. (2009). Meis cofactors control HDAC and CBP accessibility at Hox-regulated promoters during zebrafish embryogenesis. Dev. Cell 17, 561-567.
7. Cobb, J.,Dierich, A.,Huss-Garcia, Y. and Duboule, D. (2006). A mouse model for human short-stature syndromes identifies Shox2 as an upstream regulator of Runx2 during long-bone development. Proc. Natl. Acad. Sci. USA 103, 4511-4515.
8. Colnot, C.,Lu, C.,Hu, D. and Helms, J. A. (2004). Distinguishing the contributions of the perichondrium, cartilage, and vascular endothelium to skeletal development. Dev. Biol. 269, 55-69.
9. Crocker, J.,Abe, N.,Rinaldi, L.,McGregor, A. P.,Frankel, N.,Wang, S.,Alsawadi, A.,Valenti, P.,Plaza, S.,Payre, F. et al. (2015). Low affinity binding site clusters confer hox specificity and regulatory robustness. Cell 160, 191-203.
10. Cunningham, T. J. and Duester, G. (2015). Mechanisms of retinoic acid signaling and its roles in organ and limb development. Nat. Rev. Mol. Cell Biol. 16, 110-123.
11. Dixon, J. R.,Selvaraj, S.,Yue, F.,Kim, A.,Li, Y.,Shen, Y.,Hu, M.,Liu, J. S. and Ren, B. (2012). Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380.
12. Espinoza-Lewis, R. A.,Yu, L.,He, F.,Liu, H.,Tang, R.,Shi, J.,Sun, X.,Martin, J. F.,Wang, D.,Yang, J. et al. (2009). Shox2 is essential for the differentiation of cardiac pacemaker cells by repressing Nkx2-5. Dev. Biol. 327, 376-385.
13. Gordon, J. A. R.,Hassan, M. Q.,Saini, S.,Montecino, M.,van Wijnen, A. J.,Stein, G. S.,Stein, J. L. and Lian, J. B. (2010). Pbx1 represses osteoblastogenesis by blocking Hoxa10-mediated recruitment of chromatin remodeling factors. Mol. Cell. Biol. 30, 3531-3541.
14. Gu, S.,Wei, N.,Yu, X.,Jiang, Y.,Fei, J. and Chen, Y. (2008). Mice with an anterior cleft of the palate survive neonatal lethality. Dev. Dyn. 237, 1509-1516.
15. Huang, Y.,Sitwala, K.,Bronstein, J.,Sanders, D.,Dandekar, M.,Collins, C.,Robertson, G.,MacDonald, J.,Cezard, T.,Bilenky, M. et al. (2012). Identification and characterization of Hoxa9 binding sites in hematopoietic cells. Blood 119, 388-398.
16. Hudry, B.,Thomas-Chollier, M.,Volovik, Y.,Duffraisse, M.,Dard, A.,Frank, D.,Technau, U. and Merabet, S. (2014). Molecular insights into the origin of the Hox-TALE patterning system. Elife 3, e01939.
17. Infante, C. R.,Park, S.,Mihala, A. G.,Kingsley, D. M. and Menke, D. B. (2013). Pitx1 broadly associates with limb enhancers and is enriched on hindlimb cis-regulatory elements. Dev. Biol. 374, 234-244.
18. Jolma, A.,Yin, Y.,Nitta, K. R.,Dave, K.,Popov, A.,Taipale, M.,Enge, M.,Kivioja, T.,Morgunova, E. and Taipale, J. (2015). DNA-dependent formation of transcription factor pairs alters their binding specificity. Nature 527, 384-388.
19. Kmita, M.,Tarchini, B.,Zakany, J.,Logan, M.,Tabin, C. J. and Duboule, D. (2005). Early developmental arrest of mammalian limbs lacking HoxA/HoxD gene function. Nature 435, 1113-1116.
20. Kondrashov, N.,Pusic, A.,Stumpf, C. R.,Shimizu, K.,Hsieh, A. C.,Xue, S.,Ishijima, J.,Shiroishi, T. and Barna, M. (2011). Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145, 383-397.
21. Liu, F.,Woitge, H. W.,Braut, A.,Kronenberg, M. S.,Lichtler, A. C.,Mina, M. and Kream, B. E. (2004). Expression and activity of osteoblast-targeted Cre recombinase transgenes in murine skeletal tissues. Int. J. Dev. Biol. 48, 645-653.
22. Long, F. and Ornitz, D. M. (2013). Development of the endochondral skeleton. Cold Spring Harb. Perspect. Biol. 5, a008334.
23. Mann, R. S.,Lelli, K. M. and Joshi, R. (2009). Hox specificity: unique roles for cofactors and collaborators. Curr. Top. Dev. Biol. 88, 63-101.
24. Mercader, N.,Leonardo, E.,Piedra, M. E.,Martinez, A. C.,Ros, M. A. and Torres, M. (2000). Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development 127, 3961-3970.
25. Mercader, N.,Selleri, L.,Criado, L. M.,Pallares, P.,Parras, C.,Cleary, M. L. and Torres, M. (2009). Ectopic Meis1 expression in the mouse limb bud alters P-D patterning in a Pbx1-independent manner. Int. J. Dev. Biol. 53, 1483-1494.
26. Moens, C. B. and Selleri, L. (2006). Hox cofactors in vertebrate development. Dev. Biol. 291, 193-206.
27. Montavon, T.,Soshnikova, N.,Mascrez, B.,Joye, E.,Thevenet, L.,Splinter, E.,de Laat, W.,Spitz, F. and Duboule, D. (2011). A regulatory archipelago controls Hox genes transcription in digits. Cell 147, 1132-1145.
28. Neufeld, S. J.,Wang, F. and Cobb, J. (2014). Genetic interactions between Shox2 and Hox genes during the regional growth and development of the mouse limb. Genetics 198, 1117-1126.
29. Ohbayashi, N.,Shibayama, M.,Kurotaki, Y.,Imanishi, M.,Fujimori, T.,Itoh, N. and Takada, S. (2002). FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev. 16, 870-879.
30. Osterwalder, M.,Speziale, D.,Shoukry, M.,Mohan, R.,Ivanek, R.,Kohler, M.,Beisel, C.,Wen, X.,Scales, S. J.,Christoffels, V. M. et al. (2014). HAND2 targets define a network of transcriptional regulators that compartmentalize the early limb bud mesenchyme. Dev. Cell 31, 345-357.
31. Ovchinnikov, D. A.,Deng, J. M.,Ogunrinu, G. and Behringer, R. R. (2000). Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis 26, 145-146.
32. Parker, H. J.,Piccinelli, P.,Sauka-Spengler, T.,Bronner, M. and Elgar, G. (2011). Ancient Pbx-Hox signatures define hundreds of vertebrate developmental enhancers. BMC Genomics 12, 637.
33. Pearson, J. C.,Lemons, D. and McGinnis, W. (2005). Modulating Hox gene functions during animal body patterning. Nat. Rev. Genet. 6, 893-904.
34. Penkov, D.,Mateos San Martin, D.,Fernandez-Diaz, L. C.,Rossello, C. A.,Torroja, C.,Sanchez-Cabo, F.,Warnatz, H. J.,Sultan, M.,Yaspo, M. L.,Gabrieli, A. et al. (2013). Analysis of the DNA-binding profile and function of TALE homeoproteins reveals their specialization and specific interactions with Hox genes/proteins. Cell Rep. 3, 1321-1333.
35. Raines, A. M.,Magella, B.,Adam, M. and Potter, S. S. (2015). Key pathways regulated by HoxA9,10,11/HoxD9,10,11 during limb development. BMC Dev. Biol. 15, 28.
36. Rosin, J. M.,Abassah-Oppong, S. and Cobb, J. (2013). Comparative transgenic analysis of enhancers from the human SHOX and mouse Shox2 genomic regions. Hum. Mol. Genet. 22, 3063-3076.
37. Shen, Y.,Yue, F.,McCleary, D. F.,Ye, Z.,Edsall, L.,Kuan, S.,Wagner, U.,Dixon, J.,Lee, L.,Lobanenkov, V. V. et al. (2012). A map of the cis-regulatory sequences in the mouse genome. Nature 488, 116-120.
38. Slattery, M.,Riley, T.,Liu, P.,Abe, N.,Gomez-Alcala, P.,Dror, I.,Zhou, T.,Rohs, R.,Honig, B.,Bussemaker, H. J. et al. (2011). Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 147, 1270-1282.
39. St John, H. C.,Bishop, K. A.,Meyer, M. B.,Benkusky, N. A.,Leng, N.,Kendziorski, C.,Bonewald, L. F. and Pike, J. W. (2014). The osteoblast to osteocyte transition: epigenetic changes and response to the vitamin D3 hormone. Mol. Endocrinol. 28, 1150-1165.
40. Sun, C.,Zhang, T.,Liu, C.,Gu, S. and Chen, Y. (2013). Generation of Shox2-Cre allele for tissue specific manipulation of genes in the developing heart, palate, and limb. Genesis 51, 515-522.
41. Swinehart, I. T.,Schlientz, A. J.,Quintanilla, C. A.,Mortlock, D. P. and Wellik, D. M. (2013). Hox11 genes are required for regional patterning and integration of muscle, tendon and bone. Development 140, 4574-4582.
42. Tabin, C. and Wolpert, L. (2007). Rethinking the proximodistal axis of the vertebrate limb in the molecular era. Genes Dev. 21, 1433-1442.
43. VanderMeer, J. E.,Smith, R. P.,Jones, S. L. and Ahituv, N. (2014). Genome-wide identification of signaling center enhancers in the developing limb. Development 141, 4194-4198.
44. Vickerman, L.,Neufeld, S. and Cobb, J. (2011). Shox2 function couples neural, muscular and skeletal development in the proximal forelimb. Dev. Biol. 350, 323-336.
45. Villavicencio-Lorini, P.,Kuss, P.,Friedrich, J.,Haupt, J.,Farooq, M.,Turkmen, S.,Duboule, D.,Hecht, J. and Mundlos, S. (2010). Homeobox genes d11-d13 and a13 control mouse autopod cortical bone and joint formation. J. Clin. Invest. 120, 1994-2004.
46. Visel, A.,Minovitsky, S.,Dubchak, I. and Pennacchio, L. A. (2007). VISTA Enhancer Browser-a database of tissue-specific human enhancers. Nucleic Acids Res. 35, D88-D92.
47. Visel, A.,Blow, M. J.,Li, Z.,Zhang, T.,Akiyama, J. A.,Holt, A.,Plajzer-Frick, I.,Shoukry, M.,Wright, C.,Chen, F. et al. (2009). ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858.
48. Vokes, S. A.,Ji, H.,Wong, W. H. and McMahon, A. P. (2008). A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev. 22, 2651-2663.
49. Wang, S.,Sun, H.,Ma, J.,Zang, C.,Wang, C.,Wang, J.,Tang, Q.,Meyer, C. A.,Zhang, Y. and Liu, X. S. (2013). Target analysis by integration of transcriptome and ChIP-seq data with BETA. Nat. Protoc. 8, 2502-2515.
50. Wang, J.,Bai, Y.,Li, N.,Ye, W.,Zhang, M.,Greene, S. B.,Tao, Y.,Chen, Y.,Wehrens, X. H. T. and Martin, J. F. (2014). Pitx2-microRNA pathway that delimits sinoatrial node development and inhibits predisposition to atrial fibrillation. Proc. Natl. Acad. Sci. USA 111, 9181-9186.
51. Wu, H.,Whitfield, T. W.,Gordon, J. A. R.,Dobson, J. R.,Tai, P. W. L.,van Wijnen, A. J.,Stein, J. L.,Stein, G. S. and Lian, J. B. (2014). Genomic occupancy of Runx2 with global expression profiling identifies a novel dimension to control of osteoblastogenesis. Genome Biol. 15, R52.
52. Ye, W.,Song, Y.,Huang, Z.,Zhang, Y. and Chen, Y. (2015a). Genetic regulation of sinoatrial node development and pacemaker program in the venous pole. J. Cardiovasc. Dev. Dis. 2, 282-298.
53. Ye, W.,Wang, J.,Song, Y.,Yu, D.,Sun, C.,Liu, C.,Chen, F.,Zhang, Y.,Wang, F.,Harvey, R. P. et al. (2015b). A common Shox2-Nkx2-5 antagonistic mechanism primes the pacemaker cell fate in the pulmonary vein myocardium and sinoatrial node. Development 142, 2521-2532.
54. Yu, L.,Gu, S.,Alappat, S.,Song, Y.,Yan, M.,Zhang, X.,Zhang, G.,Jiang, Y.,Zhang, Z.,Zhang, Y. et al. (2005). Shox2-deficient mice exhibit a rare type of incomplete clefting of the secondary palate. Development 132, 4397-4406.
55. Yu, L.,Liu, H.,Yan, M.,Yang, J.,Long, F.,Muneoka, K. and Chen, Y. (2007). Shox2 is required for chondrocyte proliferation and maturation in proximal limb skeleton. Dev. Biol. 306, 549-559.
56. Yue, F.,Cheng, Y.,Breschi, A.,Vierstra, J.,Wu, W.,Ryba, T.,Sandstrom, R.,Ma, Z.,Davis, C.,Pope, B. D. et al. (2014). A comparative encyclopedia of DNA elements in the mouse genome. Nature 515, 355-364.
57. Zakany, J. and Duboule, D. (2007). The role of Hox genes during vertebrate limb development. Curr. Opin. Genet. Dev. 17, 359-366.