Regulation of Sox9 by Sonic Hedgehog (Shh) is essential for patterning and formation of tracheal cartilage

Developmental Dynamics

Volumn 239, Issue 2, 2010, Pages 514-526

  Park, Jinhyung ^a   Zhang, Jennifer J R ^a   Moro, Anne ^b   Kushida, Michelle ^a   Wegner, Michael ^c   Kim, Peter C W ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Mouse; Shh; Sox9; Tracheal cartilage

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CYCLOPAMINE; NOGGIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR SOX9;

ANIMAL TISSUE; ARTICLE; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRACHEA;

ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEIN 4; CARRIER PROTEINS; CELL PROLIFERATION; CHONDROGENESIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LARYNGEAL CARTILAGES; MICE; MICE, KNOCKOUT; SOX9 TRANSCRIPTION FACTOR;

ERINACEIDAE;

EID: 75149152434     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22192     Document Type: Article

References (46)

1. Akiyama H, Chaboissier MC, Martin JF, Schedl A, de Crombrugghe B. 2002. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 16:2813-2828.
2. Bai CB, Auerbach W, Lee JS, Stephen D, Joyner AL. 2002. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129:4753-4761.
3. Barbieri O, Astigiano S, Morini M, Tavella S, Schito A, Corsi A, Di Martino D, Bianco P, Cancedda R, Garofalo S. 2003. Depletion of cartilage collagen fibrils in mice carrying a dominant negative Col2a1 transgene affects chondrocyte differentiation. Am J Physiol Cell Physiol 285:C1504-1512.
4. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PP, Cheah KS. 1997. SOX9 directly regulates the type-II collagen gene. Nat Genet 16:174-178.
5. Bi W, Huang W, Whitworth DJ, Deng JM, Zhang Z, Behringer RR, de Crom-brugghe B. 2001. Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc Natl Acad Sci USA 98: 6698-6703.
6. Bien-Willner GA, Stankiewicz P, Lupski JR. 2007. SOX9cre1, a cis-acting regulatory element located 1.1 Mb upstream of SOX9, mediates its enhancement through the SHH pathway. Hum Mol Genet 16:1143-1156.
7. Capdevila J, Johnson RL. 1998. Endogenous and ectopic expression of noggin suggests a conserved mechanism for regulation of BMP function during limb and somite patterning. Dev Biol 197: 205-217.
8. Chen JK, Taipale J, Cooper MK, Beachy PA. 2002. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev 16: 2743-2748.
9. Cooper MK, Porter JA, Young KE, Beachy PA. 1998. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science 280:1603-1607.
10. Dahmane N, Sanchez P, Gitton Y, Palma V, Sun T, Beyna M, Weiner H, Ruiz i Altaba A. 2001. The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumorigenesis. Development 128:5201-5212.
11. de Crombrugghe B, Lefebvre V, Nakashima K. 2001. Regulatory mechanisms in the pathways of cartilage and bone formation. Curr Opin Cell Biol 13: 721-727.
12. Duprez D, Bell EJ, Richardson MK, Archer CW, Wolpert L, Brickell PM, Francis-West PH. 1996. 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.
13. Elluru RG, Whitsett JA. 2004. Potential role of Sox9 in patterning tracheal cartilage ring formation in an embryonic mouse model. Arch Otolaryngol Head Neck Surg 130:732-736.
14. Faust RA, Stroh B, Rimell F. 1998. The near complete tracheal ring deformity. Int J Pediatr Otorhinolaryngol 45: 171-176.
15. Gillotte DM, Fox PL, Mjaatvedt CH, Hoffman S, Capehart AA. 2003. An in vitro method for analysis of chondrogenesis in limb mesenchyme from individual transgenic (hdf) embryos. Methods Cell Sci 25:97-104.
16. Hasaniya N, elZein CF, Mara S, Barth MJ, Ilbawi M. 2006. Alternative approach to the surgical management of congenital tracheal stenosis. Ann Thorac Surg 82:2305-2307.
17. Hui CC, Joyner AL. 1993. A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat Genet 3:241-246.
18. Krengel S, Gotz W, Herken R. 1996. Expression pattern of type II collagen mRNA during early vertebral development in the human embryo. Anat Embryol (Berl) 193:43-51.
19. Litingtung Y, Lei L, Westphal H, Chiang C. 1998. Sonic hedgehog is essential to foregut development. Nat Genet 20: 58-61.
20. Lopez-Martinez A, Chang DT, Chiang C, Porter JA, Ros MA, Simandl BK, Beachy PA, Fallon JF. 1995. Limb-patterning activity and restricted posterior localization of the amino-terminal product of Sonic hedgehog cleavage. Curr Biol 5:791-796.
21. McAteer JA. 1984. Tracheal morphogenesis and fetal development of the mucociliary epithelium of the rat. Scan Electron Microsc 1984:1995-2008.
22. Mill P, Mo R, Fu H, Grachtchouk M, Kim PC, Dlugosz AA, Hui CC. 2003. Sonic hedgehog-dependent activation of Gli2 is essential for embryonic hair follicle development. Genes Dev 17:282-294.
23. Miller LA, Wert SE, Clark JC, Xu Y, Perl AK, Whitsett JA. 2004. Role of Sonic hedgehog in patterning of trachealbronchial cartilage and the peripheral lung. Dev Dyn 231:57-71.
24. Minoo P, Su G, Drum H, Bringas P, Kimura S. 1999. Defects in tracheoesophageal and lung morphogenesis in Nkx2.1(-/-) mouse embryos. Dev Biol 209:60-71.
25. Motoyama J, Liu J, Mo R, Ding Q, Post M, Hui CC. 1998. Essential function of Gli2 and Gli3 in the formation of lung, trachea and oesophagus. Nat Genet 20: 54-57.
26. Nagase T, Nagase M, Osumi N, Fukuda S, Nakamura S, Ohsaki K, Harii K, Asato H, Yoshimura K. 2005. Craniofacial anomalies of the cultured mouse embryo induced by inhibition of sonic hedgehog signaling: an animal model of holoprosencephaly. J Craniofac Surg 16:80-88.
27. Nifuji A, Kellermann O, Noda M. 2004. Noggin inhibits chondrogenic but not osteogenic differentiation in mesodermal stem cell line C1 and skeletal cells. Endocrinology 145:3434-3442.
28. Nifuji A, Noda M. 1999. Coordinated expression of noggin and bone morphogenetic proteins (BMPs) during early skeletogenesis and induction of noggin expression by BMP-7. J Bone Miner Res 14:2057-2066.
29. Pathi S, Rutenberg JB, Johnson RL, Vortkamp A. 1999. Interaction of Ihh and BMP/Noggin signaling during cartilage differentiation. Dev Biol 209:239-253.
30. Perl AK, Wert SE, Nagy A, Lobe CG, Whitsett JA. 2002. Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc Natl Acad Sci USA 99:10482-10487.
31. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
32. Pizette S, Niswander L. 2000. BMPs are required at two steps of limb chondrogenesis: formation of prechondrogenic condensations and their differentiation into chondrocytes. Dev Biol 219:237-249.
33. Que J, Choi M, Ziel JW, Klingensmith J, Hogan BL. 2006. Morphogenesis of the trachea and esophagus: current players and new roles for noggin and Bmps. Differentiation 74:422-437.
34. Rutter MJ, Vijayasekaran S, Salamone FN, Cohen AP, Manning P, Collins MH, Mortelliti A. 2006. Deficient tracheal rings. Int J Pediatr Otorhinolaryngol 70:1981-1984.
35. Sanchez P, Hernandez AM, Stecca B, Kahler AJ, DeGueme AM, Barrett A, Beyna M, Datta MW, Datta S, Ruiz i Altaba A. 2004. Inhibition of prostate cancer proliferation by interference with SONIC HEDGEHOG-GLI1 signaling. Proc Natl Acad Sci USA 101:12561-12566.
36. Schell-Apacik C, Rivero M, Knepper JL, Roessler E, Muenke M, Ming JE. 2003. SONIC HEDGEHOG mutations causing human holoprosencephaly impair neural patterning activity. Hum Genet 113: 170-177.
37. Shum L, Wang X, Kane AA, Nuckolls GH. 2003. BMP4 promotes chondrocyte proliferation and hypertrophy in the endochondral cranial base. Int J Dev Biol 47:423-431.
38. Tacchetti C, Tavella S, Dozin B, Quarto R, Robino G, Cancedda R. 1992. Cell condensation in chondrogenic differentiation. Exp Cell Res 200:26-33.
39. Tavella S, Biticchi R, Schito A,Minina E, Di Martino D, Pagano A, Vortkamp A, Horton WA, Cancedda R, Garofalo S. 2004. Targeted expression of SHH affects chondrocyte differentiation, growth plate organization, and Sox9 expression. J Bone Miner Res 19:1678-1688.
40. Thibert C, Teillet MA, Lapointe F, Mazelin L, Le Douarin NM, Mehlen P. 2003. Inhibition of neuroepithelial patchedinduced apoptosis by sonic hedgehog. Science 301:843-846.
41. Tsumaki N, Nakase T, Miyaji T, Kakiuchi M, Kimura T, Ochi T, Yoshikawa H. 2002. Bone morphogenetic protein signals are required for cartilage formation and differently regulate joint development during skeletogenesis. J Bone Miner Res 17:898-906.
42. Villavicencio EH, Walterhouse DO, Iannaccone PM. 2000. The sonic hedgehogpatched-gli pathway in human development and disease. Am J Hum Genet 67: 1047-1054.
43. Weaver M, Yingling JM, Dunn NR, Bellusci S, Hogan BL. 1999. Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development. Development 126:4005-4015.
44. Weaver M, Batts L, Hogan BL. 2003. Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev Biol 258:169-184.
45. Zehentner BK, Haussmann A, Burtscher H. 2002. The bone morphogenetic protein antagonist Noggin is regulated by Sox9 during endochondral differentiation. Dev Growth Differ 44:1-9.
46. Zeng L, Kempf H, Murtaugh LC, Sato ME, Lassar AB. 2002. Shh establishes an Nkx3.2/Sox9 autoregulatory loop that is maintained by BMP signals to induce somitic chondrogenesis. Genes Dev 16:1990-2005.