Long bone development requires a threshold of Hox function

Developmental Biology

Volumn 392, Issue 2, 2014, Pages 454-465

  González Martín, M Carmen ^a   Mallo, Moises ^b   Ros, Marian A ^a  

^a UNIVERSITY OF CANTABRIA   (Spain)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

Chondrogenesis; Gli3; Hoxd genes; Ihh; Osteogenesis; Short bones

Indexed keywords

HOX PROTEIN; TRANSCRIPTION FACTOR GLI3;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE DEVELOPMENT; BONE MATURATION; CARTILAGE CELL; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; GENE; GENE EXPRESSION; GROWTH PLATE; HETEROZYGOSITY; HOMOZYGOSITY; HOX GENE; IHH GENE; LONG BONE; METACARPAL BONE; METATARSAL BONE; MOUSE; NONHUMAN; OSSIFICATION; PERINATAL PERIOD; PHALANX; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL;

ANIMALIA;

CHONDROGENESIS; GLI3; HOXD GENES; IHH; OSTEOGENESIS; SHORT-BONES;

ANIMALS; BLOTTING, WESTERN; BONE DEVELOPMENT; DISEASE MODELS, ANIMAL; DNA PRIMERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HISTOLOGICAL TECHNIQUES; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, MUTANT STRAINS; MUTATION; NERVE TISSUE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; SYNDACTYLY;

EID: 84904391423     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.06.004     Document Type: Article

References (67)

1. Albrecht A.N., Schwabe G.C., Stricker S., Boddrich A., Wanker E.E, Mundlos S. The synpolydactyly homolog (spdh) mutation in the mouse-a defect in patterning and growth of limb cartilage elements. Mech. Dev. 2002, 112:53-67.
2. Boulet A.M., Capecchi M.R. Multiple roles of Hoxa11 and Hoxd11 in the formation of the mammalian forelimb zeugopod. Development 2004, 131:299-309.
3. Brison N., Debeer P., Tylzanowski P. Joining the fingers-a HOXD13 story. Dev. Dyn. 2014.
4. Bruneau S., Johnson K.R., Yamamoto M., Kuroiwa A., Johnson K.R., Yamamoto M., Kuroiwa A., Duboule D. The mouse Hoxd13(spdh) mutation, a polyalanine expansion similar to human type II synpolydactyly (SPD), disrupts the function but not the expression of other Hoxd genes. Dev. Biol. 2001, 237:345-353.
5. Capellini T.D., Di Giacomo G., Salsi V., Brendolan A., Ferretti E., Srivastava D., Zappavigna V., Selleri L. Pbx1/Pbx2 requirement for distal limb patterning is mediated by the hierarchical control of Hox gene spatial distribution and Shh expression. Development 2006, 133:2263-2273.
6. Chen Y., Knezevic V., Ervin V., Hutson R., Ward Y., Mackem S. Direct interaction with Hoxd proteins reverses Gli3-repressor function to promote digit formation downstream of Shh. Development 2004, 131:2339-2347.
7. Chiang C., Litingtung Y., Harris M.P., Simandl B.K., Li Y., Beachy P.A., Fallon J.F. Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev. Biol. 2001, 236:421-435.
8. Chung U.I., Schipani E., McMahon A.P., Kronenberg H.M. Indian hedgehog couples chondrogenesis to osteogenesis in endochondral bone development. J. Clin. Invest. 2001, 107:295-304.
9. Dao D.Y., Yang X., Flick L.M., Chen D., Hilton M.J., O'Keefe R.J. Axin2 regulates chondrocyte maturation and axial skeletal development. J. Orthop. Res. 2009, 28:89-95.
10. Davis A.P., Capecchi M.R. Axial homeosis and appendicular skeleton defects in mice with a targeted disruption of hoxd-11. Development 1994, 120:2187-2198.
11. Davis A.P., Capecchi M.R. A mutational analysis of the 5' HoxD genes: dissection of genetic interactions during limb development in the mouse. Development 1996, 122:1175-1185.
12. de Crombrugghe B., Lefebvre V., Nakashima K. Regulatory mechanisms in the pathways of cartilage and bone formation. Curr. Opin. Cell Biol. 2001, 13:721-727.
13. Dolle P., Izpisua-Belmonte J.C., Brown J., Tickle C., Duboule D. Hox genes and the morphogenesis of the vertebrate limb. Prog. Clin. Biol. Res 1993, 383A:11-20.
14. Erlebacher A., Filvaroff E.H., Gitelman S.E., Derynck R. Toward a molecular understanding of skeletal development. Cell 1995, 80:371-378.
15. Fromental-Ramain C., Warot X., Messadecq N., LeMeur M., Dollé P., Chambon P. Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 1996, 122:2997-3011.
16. Gersch R.P., Lombardo F., McGovern S.C., Hadjiargyrou M. Reactivation of Hox gene expression during bone regeneration. J. Orthop. Res. 2005, 23:882-890.
17. Goff D.J., Tabin C.J. Analysis of Hoxd-13 and Hoxd-11 misexpression in chick limb buds reveals that Hox genes affect both bone condensation and growth. Development 1997, 124:627-636.
18. Gross S., Krause Y., Wuelling M., Vortkamp A. Hoxa11 and Hoxd11 regulate chondrocyte differentiation upstream of Runx2 and Shox2 in mice. PLoS One 2012, 7:e43553. http://dx.doi.org/10.1371/journal.pone.0043553, PMID: 22916278 [PubMed - indexed for MEDLINE].
19. Hassan M.Q., Tare R., Lee S.H., Mandeville M., Weiner B., Montecino M., van Wijnen A.J., Stein J.L., Stein G.S., Lian J.B. HOXA10 controls osteoblastogenesis by directly activating bone regulatory and phenotypic genes. Mol. Cell. Biol. 2007, 27:3337-3352.
20. Hilton M.J., Tu X., Cook J., Hu H., Long F. Ihh controls cartilage development by antagonizing Gli3, but requires additional effectors to regulate osteoblast and vascular development. Development 2005, 132:4339-4351.
21. Hui C.C., Joyner A.L. A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet. 1993, 3:241-246.
22. Joeng K.S., Long F. The Gli2 transcriptional activator is a crucial effector for Ihh signaling in osteoblast development and cartilage vascularization. Development 2009, 136:4177-4185.
23. Johnson K.R., Sweet H.O., Donahue L.R., Ward-Bailey P., Bronson R.T., Davisson M.T. A new spontaneous mouse mutation of Hoxd13 with a polyalanine expansion and phenotype similar to human synpolydactyly. Hum. Mol. Genet. 1998, 7:1033-1038.
24. Karp S.J., Schipani E., St-Jacques B., Hunzelman J., Kronenberg H., McMahon A.P. Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone related-protein-dependent and -independent pathways. Development 2000, 127:543-548.
25. Karsenty G. Chondrogenesis just ain't what it used to be. J. Clin. Invest. 2001, 107:405-407.
26. Karsenty G. Transcriptional control of skeletogenesis. Annu. Rev. Genomics Hum. Genet 2008, 9:183-196.
27. Karsenty G., Kronenberg H.M., Settembre C. Genetic control of bone formation. Annu. Rev. Cell Dev. Biol. 2009, 25:629-648.
28. Kesper D.A., Didt-Koziel L., Vortkamp A. Gli2 activator function in preosteoblasts is sufficient to mediate Ihh-dependent osteoblast differentiation, whereas the repressor function of Gli2 is dispensable for endochondral ossification. Dev. Dyn. 2010, 239(6):1818-1826. 10.1002/dvdy.22301.
29. Kim I.S., Otto F., Zabel B., Mundlos S. Regulation of chondrocyte differentiation by Cbfa1. Mech. Dev. 1999, 80(2):159-170.
30. Knosp W.M., Scott V., Bachinger H.P., Stadler H.S. HOXA13 regulates the expression of bone morphogenetic proteins 2 and 7 to control distal limb morphogenesis. Development 2004, 131:4581-4592.
31. Kobayashi T, Kronenberg H.M. Overview of skeletal development. Methods Mol. Biol. 2014, 1130:3-12.
32. Koziel L., Wuelling M., Schneider S., Vortkamp A. Gli3 acts as a repressor downstream of Ihh in regulating two distinct steps of chondrocyte differentiation. Development 2005, 132:5249-5260.
33. Krumlauf R. Hox genes in vertebrate development. Cell 1994, 78:191-201.
34. Kuss P., Kuss P., Kraft K., Stumm J., Ibrahim D., Vallecillo-Garcia P., Mundlos S., Stricker S. Regulation of cell polarity in the cartilage growth plate and perichondrium of metacarpal elements by HOXD13 and WNT5A. Dev. Biol. 2013, 385:83-93.
35. Lanske B., Karaplis A.C., Lee K., Luz A., Vortkamp A., Pirro A., Karperien M., Defize L.H., Ho C., Mulligan R.C., Abou-Samra A.B., Juppner H., Segre G.V., Kronenberg H.M. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science 1996, 273:663-666.
36. Lee K., Lanske B., Karaplis A.C., Deeds J.D., Kohno H., Nissenson R.A., Kronenberg H.M., Segre G.V. Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology 1996, 137:5109-5118.
37. Long F., Chung U.I., Ohba S., McMahon J., Kronenberg H.M., McMahon A.P. Ihh signaling is directly required for the osteoblast lineage in the endochondral skeleton. Development 2004, 131:1309-1318.
38. Long F., Zhang.X.M., Karp.S., Yang.Y., McMahon.A.P. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 2001, 128:5099-5108.
39. Mak K.K., Kronenberg H.M., Chuang P.T., Mackem S., Yang Y. Indian hedgehog signals independently of PTHrP to promote chondrocyte hypertrophy. Development 2008, 135:1947-1956.
40. Mallo M., Wellik D.M., Deschamps J. Hox genes and regional patterning of the vertebrate body plan. Dev. Biol. 2010, 344:7-15.
41. Massip L., Ectors F., Deprez P., Maleki M., Behets C., Lengele B., Delahaut P., Picard J., Rezsohazy R. Expression of Hoxa2 in cells entering chondrogenesis impairs overall cartilage development. Differentiation 2007, 75:256-267.
42. McLeod M.J. Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 1980, 22:299-301.
43. Minina E., Schneider S., Rosowski M., Lauster R., Vortkamp A. Expression of Fgf and Tgfbeta signaling related genes during embryonic endochondral ossification. Gene Expression Patterns 2005, 6:102-109.
44. Montavon T., Le Garrec J.F., Kerszberg M., Duboule D. Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness. Genes Dev. 2008, 22:346-359.
45. Morgan B.A., Izpisua-Belmonte J.C., Duboule D., Tabin C.J. Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 1992, 358:236-239.
46. Rodda S.J., McMahon A.P. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 2006, 133:3231-3244.
47. Sheth R., Bastida M.F., Kmita M., Ros M. "Self-regulation," a new facet of Hox genes' function. Dev. Dyn. 2014.
48. Sheth R., Marcon L., Bastida M.F., Junco M., Quintana L., Dahn R., Kmita M., Sharpe J., Ros M.A. Hoxd and Gli3 interactions modulate digit number in the amniote limb. Dev. Biol. 2007, 310:430-441.
49. Sheth R., Gregoire D., Dumouchel A., Scotti M., Pham J.M., Nemec S., Bastida M.F., Ros M.A., Kmita M. Decoupling the function of Hox and Shh in developing limb reveals multiple inputs of Hox genes on limb growth. Development 2013, 140:2130-2138.
50. Sheth R., Bastida M.F., Ros M. Hox genes regulate digit patterning by controlling the wavelength of a Turing-type mechanism. Science 2012, 338:1476-1480.
51. Spater D., Hill T.P., O'Sullivan R J., Gruber M., Conner D.A., Hartmann C. Wnt9a signaling is required for joint integrity and regulation of Ihh during chondrogenesis. Development 2006, 133:3039-3049.
52. St-Jacques B., Hammerschmidt M., McMahon A.P. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 1999, 13:2072-2086.
53. Stricker S., Fundele R., Vortkamp A., Mundlos S. Role of Runx genes in chondrocyte differentiation. Dev. Biol. 2002, 245:95-108.
54. Takamoto M., Tsuji K., Yamashita T., Sasaki H., Yano T., Taketani Y., Komori T., Nifuji A., Noda M. Hedgehog signaling enhances core-binding factor a1 and receptor activator of nuclear factor-kappaB ligand (RANKL) gene expression in chondrocytes. J. Endocrinol. 2003, 177:413-421.
55. Vargas A.O., Fallon J.F. The digits of the wing of birds are 1, 2, and 3. A review. J. Exp. Zool. B: Mol. Dev. Evol 2005, 304:206-219.
56. Vargas A.O., Wagner G.P. Frame-shifts of digit identity in bird evolution and Cyclopamine-treated wings. Evol. Dev. 2009, 11:163-169.
57. Villavicencio-Lorini P., Kuss P., Friedrich J., Haupt J., Farooq M., Turkmen S., Duboule D., Hecht J., Mundlos S. Homeobox genes d11-d13 and a13 control mouse autopod cortical bone and joint formation. J. Clin. Invest. 2010, 120:1994-2004.
58. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273:613-622.
59. Wen X., Lai C.K., Evangelista M., Hongo J.A., de Sauvage F.J., Scales S.J. Kinetics of hedgehog-dependent full-length Gli3 accumulation in primary cilia and subsequent degradation. Mol. Cell. Biol. 2010, 30:1910-1922.
60. Wellik D.M., Capecchi M.R. Hox10 and Hox11 genes are required to globally pattern the mammalian skeleton. Science 2003, 18;301(5631):363-367.
61. Woltering J.M., Duboule D. The origin of digits: expression patterns versus regulatory mechanisms. Dev. Cell. 2010, 18:526-532.
62. Yokouchi Y., Nakazato S., Yamamoto M., Goto Y., Kameda T., Iba H., Kuroiwa A. Misexpression of Hoxa-13 induces cartilage homeotic transformation and changes cell adhesiveness in chick limb buds. Genes Dev. 1995, 9:2509-2522.
63. Yoshida C.A., Yamamoto H., Fujita T., Furuichi T., Ito K., Inoue K., Yamana K., Zanma A., Takada K., Ito Y., Komori T. Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev. 2004, 18:952-963.
64. Yucel A., Kuru I, Bozan M.E., Acar M., Solak M. Radiographic evaluation and unusual bone formations in different genetic patterns in synpolydactyly. Skeletal Radiol. 2005, 34:468-476.
65. Yueh Y.G., Gardner D.P., Kappen C. Evidence for regulation of cartilage differentiation by the homeobox gene Hoxc-8. Proc. Nat. Acad. Sci. U.S.A 1998, 95:9956-9961.
66. Zakany J., Duboule D. Synpolydactyly in mice with a targeted deficiency in the HoxD complex. Nature 1996, 384:69-71.
67. Zakany J., Duboule D. The role of Hox genes during vertebrate limb development. Curr. Opin. Genet. Dev 2007, 17:359-366.