Directed Bmp4 expression in neural crest cells generates a genetic model for the rare human bony syngnathia birth defect

Developmental Biology

Volumn 391, Issue 2, 2014, Pages 170-181

  He, Fenglei ^a   Hu, Xuefeng ^b   Xiong, Wei ^c,f   Li, Lu ^c,g   Lin, Lisong ^d   Shen, Bin ^b   Yang, Ling ^c,e   Gu, Shuping ^c,h   Zhang, Yanding ^b   Chen, YiPing ^b,c  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b FUJIAN NORMAL UNIVERSITY   (China)

^c Tulane University   (United States)

^d FUJIAN MEDICAL UNIVERSITY   (China)

^e SUN YAT SEN UNIVERSITY   (China)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g WUHAN UNIVERSITY   (China)

^h Shanghai Research Center for Biomodel Organisms   (China)

Author keywords

Bmp signaling; Cleft palate; Cranial neural crest; Craniofacial patterning; Syngnathia

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BARX1 GENE; BIRTH DEFECT; CARTILAGE; CELL DIFFERENTIATION; CELL PROLIFERATION; CLEFT PALATE; CONGENITAL BONY SYNGNATHIA; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; DLX2 GENE; EMBRYO; FEMALE; FGF8 GENE; FOXC2 GENE; GAIN OF FUNCTION MUTATION; GENE; GENE EXPRESSION; GENETIC MODEL; HAND2 GENE; MANDIBLE; MAXILLA; MOUSE; MSX1 GENE; NEURAL CREST CELL; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALIA; MUS;

BMP SIGNALING; CLEFT PALATE; CRANIAL NEURAL CREST; CRANIOFACIAL PATTERNING; SYNGNATHIA;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CLEFT PALATE; FACIAL BONES; HUMANS; JAW ABNORMALITIES; MANDIBLE; MAXILLA; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, GENETIC; NEURAL CREST; SIGNAL TRANSDUCTION; WNT1 PROTEIN;

EID: 84901443839     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.04.013     Document Type: Article

References (68)

1. Abzhanov A., Protas M., Grant B.R., Grant P.R., Tabin C.J. Bmp4 and morphological variation of beaks in Darwin[U+05F3]s finches. Science 2004, 305:1462-1465.
2. Alappat S.R., Zhang Z., Suzuki K., Zhang X., Liu H., Jiang R., Yamada G., Chen Y. The cellular and molecular etiology of the cleft secondary palate in Fgf10 mutant mice. Dev. Biol. 2005, 277:102-113.
3. Albertson R.C., Streelman J.T., Kocher T.D., Yelick P.C. Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies. Proc. Nat. Acad. Sci. U.S.A. 2005, 102:16287-16292.
4. Anderson R.M., Stottmann R.W., Choi M., Klingensmith J. Endogenous bone morphogenetic protein antagonists regulate mammalian neural crest generation and survival. Dev. Dyn. 2006, 235:2507-2520.
5. Balemans W., Van Hul W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 2002, 250:231-250.
6. Baleato R.M., Aitken R.J., Roman S.D. Vatamin A regulation of BMP4 expression in the male germ line. Dev. Biol. 2005, 286:78-90.
7. Bandyopadhyay A., Yadav P.S., Prashar P. BMP signaling in development and diseases: a pharmacological perspective. Biochem. Pharmacol. 2013, 85:857-864.
8. Baroffio A., Dupin E., Le Douarin N.M. Common precursors for neural and mesectodermal derivatives in the cephalic neural crest. Development 1991, 112:301-305.
9. Boell L., Pallares L.F., Brodski C., Chen Y., Christian J.L., Kousa Y.A., Kuss P., Nelsen S., Novikov O., Schutte B.C., Wang Y., Tautz D. Exploring the effects of gene dosage on mandible shape in mice as a model for studying the genetic basis of natural variation. Dev. Genes Evol. 2013, 223:279-287.
10. Botchkarev V.A., Sharov A.A. BMP signaling in the control of skin development and hair follicle growth. Differentiation 2004, 72:512-526.
11. Broome M., Vial Y., Jacquemont S., Sergi C., Kamnasaran D., Giannoni E. Complete maxillo-mandibular syngnathia in a newborn with multiple congenital malformations. Pediatr. Neonatol. 2013.
12. Chai Y., Jiang X., Ito Y., Bringas P., Han J., Rowitch D.H., Soriano P., McMahon A.P., Sucov H.M. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 2000, 127:1671-1679.
13. Chai Y., Maxson R.E. Recent advances in craniofacial morphogenesis. Dev. Dyn. 2006, 235:2353-2375.
14. Chen Y., Bei M., Woo I., Satokata I., Maas R. Msx1 controls inductive signaling in mammalian tooth morphogenesis. Development 1996, 122:3035-3044.
15. Correia A.C., Costa M., Moraes F., Bom J., Novoa A., Mallo M. Bmp2 is required for migration but not for induction of neural crest cells in the mouse. Dev. Dyn. 2007, 236:2493-2501.
16. Danielian P.S., Muccino D., Rowitch D.H., Michael S.K., McMahon A.P. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 1998, 8:1323-1326.
17. Dawson K.H., Gruss J.S., Myall R.W. Congenital bone syngnathia: a proposed classification. Celft Palate Craniofac. J 1997, 34:141-146.
18. Depew M.J., Compagnucci C. Tweaking the hinge and caps: testing a model of the organization of jaws. J. Exp. Zool. B Mol. Dev. Evol. 2008, 310:315-335.
19. Depew M.J., Simpson C.A., Morasso M., Rubenstein J.L. Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J. Anat. 2005, 207:501-561.
20. Gutiérrez S.J., Gómez M., Rey J.A., Ochoa M., Gutiérrez S.M., Prieto J.C. Polymorphisms of the noggin gene and mandibular micrognathia: a first approximation. Acta Odontol. Latinoam. 2010, 23:13-19.
21. Hall B.K. The Neural Crest in Development and Evolution 1999, Springer Verlag.
22. He F., Xiong W., Wang Y., Matsui M., Yu X., Chai Y., Klingensmith J., Chen Y. Modulation of BMP signaling by Noggin is required for the maintenance of palatal epithelial integrity during palatogenesis. Dev. Biol. 2010, 347:109-121.
23. Howard M.J., Stanke M., Schneider C., Wu X., Rohrer H. The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification. Development 2000, 127:4073-4081.
24. Inman K.E., Purcell P., Kume T., Trainor P.A. Interaction between Foxc1 and Fgf8 during mammalian jaw patterning and in the pathogenesis of syngnathia. PLoS Genet. 2013, 9:e1003949.
25. Jiang X., Iseki S., Maxson R.E., Sucov H.M., Morriss-Kay G.M. Tissue origins and interactions in the mammalian skull vault. Dev. Biol. 2002, 241:106-116.
26. Kanzler B., Foreman R.K., Labosky P.A., Mallo M. BMP signaling is essential for development of skeletogenic and neurogenic cranial neural crest. Development 2000, 127:1095-1104.
27. Knoll B., Karas D., Persing J.A., Shin J. Complete congenital bony syngnathia in a case of oromandibular limb hypogenesis syndrome. J. Craniofac. Surg 2000, 11:398-404.
28. Lan Y., Wang Q., Ovitt C.E., Jiang R. A unique mouse strain expressing Cre recombinase for tissue-specific analysis of gene function in palate and kidney development. Genesis 2007, 45:618-624.
29. Le Douarin M.L., Kalcheim C. The Neural Crest 1999, Cambridge university press, London.
30. Lee S.H., Bedard O., Buchtova M., Fu K., Richman J.M. A new origin for the maxillary jaw. Dev. Biol. 2004, 276:207-224.
31. Li L., Lin M., Wang Y., Cserjesi P., Chen Z., Chen Y. BmprIa is required in mesenchymal tissue and has limited redundant function with BmprIb in tooth and palate development. Dev. Biol. 2011, 349:451-461.
32. Li L., Wang Y., Lin M., Yuan G., Yang G., Zheng Y., Chen Y. Augmented BMPRIA-mediated BMP signaling in cranial neural crest lineage leads to cleft palate formation and delayed tooth differentiation. PLoS One 2013, 8:e66107.
33. Li Y., Wang W., Yuan Z., Yang Y., Jia H., Cai W. A rapid and reliable double staining technique for mouse embryonic bone and cartilage. J. Chin. Med. Univ 2004, 23(2):189-190.
34. Liu W., Sun X., Braut A., Mishina Y., Behringer R.R., Mina M., Martin J.F. Distinct functions for Bmp signaling in lip and palate fusion in mice. Development 2005, 132:1453-1461.
35. MacKenzie B., Wolff R., Lowe N., Billington C.J., Peterson A., Schmidt B., Graf D., Mina M., Gopalakrishnan R., Petryk A. Twisted gastrulation limits apoptosis in the distal region of the mandibular arch in mice. Dev. Biol. 2009, 328:13-23.
36. Morikawa Y., Zehir A., Maska E., Deng C., Schneider M.D., Mishina Y., Cserjesi P. BMP signaling regulates sympathetic nervous system development through Smad4-dependent and -independent pathways. Development 2009, 136:3575-3584.
37. Nanda R. Maxillomandibular ankylosis and cleft palate in rat embryos. J. Dent. Res. 1970, 49:1086-1090.
38. Nie X., Luukko K., Kettunen P. BMP signalling in craniofacial development. Int. J. Dev. Biol 2006, 50:511-521.
39. Noden D.M. Cell movement and control of patterned tissue assembly during craniofacial development. J. Craniofac. Genet. Dev. Biol. 1991, 11:192-213.
40. Panchision D.M., Pickel J.M., Studer L., Lee S.H., Turner P.A., Hazel T.G., McKay R.D. Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev. 2001, 15:2094-2110.
41. Parada C., Chai Y. Roles of BMP signaling pathway in lip and palate development. Front. Oral Biol 2012, 16:60-70.
42. Parkins G.E., Boamah M.O. Congenital maxillomandibular syngnathia: case report. J. Cranio-Max.-Facial Surg 2009, 37:276-278.
43. Presnell J.K., Schreibman M.P. Humason[U+05F3]s Animal Tissue Techniques 1997, The Johns Hopkins University Press, Baltimore, MD. fifth ed.
44. Qiu M., Bulfone A., Martinez S., Meneses J.J., Shimamura K., Pedersen R.A., Rubenstein J.L. Null mutation of Dlx-2 results in abnormal morphogenesis of proximal first and second branchial arch derivatives and abnormal differentiation in the forebrain. Genes Dev. 1995, 9:2523-2538.
45. Ruest L.B., Xiang X., Lim K.C., Levi G., Clouthier D.E. Endothelin-A receptor-dependent and -independent signaling pathways in establishing mandibular identity. Development 2004, 131:4413-4423.
46. Shah J.R., Desai S.N. Congenital unilateral complex bony syngnathia with non-formation of TM joint and zygomatic arch disruption, presenting at 11 years of age. J. Cranio. Max. Dis 2013, 2:59-63.
47. Sato T., Kurihara Y., Asai R., Kawamura Y., Tonami K., Uchijima Y., Heude E., Ekker M., Levi G., Kurihara H. An endothelin-1 switch specifies maxillomandibular identity. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:18806-18811.
48. Satokata I., Maas R. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat. Genet. 1994, 6:348-356.
49. St.Amand T.R., Zhang Y., Semina E.V., Zhao X., Hu Y.P., Nguyen L., Murray J.C., Chen Y. Antagonistic signals between BMP4 and FGF8 define the expression of Pitx1 and Pitx2 in mouse tooth-forming anlage. Dev. Biol. 2000, 217:323-332.
50. Stottmann R.W., Anderson R.M., Klingensmith J. The BMP antagonists Chordin and Noggin have essential but redundant roles in mouse mandibular outgrowth. Dev. Biol. 2001, 240:457-473.
51. Stuhlmiller T.J., García-Castro M.I. Current perspectives of the signaling pathways directing neural crest induction. Cell. Mol. Life Sci. 2012, 69:3715-3737.
52. Sun J., Ishii M., Ting M.-C., Maxson R. Foxc1 controls the growth of the murine frontal bone rudiment by direct regulation of a Bmp response threshold of Msx2. Development 2013, 140:1034-1044.
53. Suzuki S., Marazita M.L., Cooper M.E., Miwa N., Hing A., Jugessur A., Natsume N., Shimozato K., Ohbayashi N., Suzuki Y., Niimi T., Minami K., Yamamoto M., Altannamar T.J., Erkhembaatar T., Furukawa H., Daack-Hirsch S., L'Heureux J., Brandon C.A., Weinberg S.M., Neiswanger K., Deleyiannis F.W., de Salamanca J.E., Vieira A.R., Lidral A.C., Martin J.F., Murray J.C. Mutations in BMP4 are associated with subepithelial, microform, and overt cleft lip. Am. J. Hum. Genet. 2009, 84:406-411.
54. Thorogood P. Differentiation and morphogenesis of cranial skeletal tissues. The Skull 1993, vol. 1:112-152. University of Chicago Press, Chicago.
55. Tissier-Seta J.P., Mucchielli M.L., Mark M., Mattei M.G., Goridis C., Brunet J.F. Barx1, a new mouse homeodomain transcription factor expressed in cranio-facial ectomesenchyme and the stomach. Mech. Dev. 1995, 51:3-15.
56. Trainor P.A. Craniofacial birth defects: the role of neural crest cells in the etiology and pathhogenesis of Treacher Collins syndrome and the potential for prevention. Am. J. Med. Genet. A 2010, 152(A):2984-2994.
57. Trainor P.A., Tam P.P.L. Cranial paraxial mesoderm and neural crest of the mouse embryo: co-distribution in the craniofacial mesenchyme but distinct segregation in branchial arches. Development 1995, 121:2569-2582.
58. Van Den Boogaard M.J., Dorland M., Beemer F.A., Van Amstel H.K. MSX1 mutation is associated with orofacial clefting and tooth agenesis in humans. Nat. Genet. 2000, 24:342-343.
59. Wu P., Jiang T.X., Suksaweang S., Widelitz R.B., Chuong C.M. Molecular shaping of the beak. Scienc 2004, 305:1465-1466.
60. Xiong W., He F., Morikawa Y., Yu X., Zhang Z., Lan Y., Jiang R., Cserjesi P., Chen Y. Hand2 is required in the epithelium for palatogenesis in mice. Dev. Biol. 2009, 330:131-141.
61. Yanagita M. BMP modulators regulate the function of BMP during body patterning and disease progression. Biofactors 2009, 35:113-119.
62. Yu L., Gu S., Alappat S., Song Y., Yan M., Zhang X., Zhang G., Jiang Y., Zhang Z., Zhang Y., Chen Y. Shox2-deficient mice exhibit a rare type of incomplete clefting of the secondary palate. Development 2005, 132:4397-4406.
63. Zhang H., Bradley A. Mice deficient for BMP2 are non-viable and have defects in amnion/chorion and cardiac development. Development 1996, 122:2977-2986.
64. Zhang Y., Zhao X., Hu Y., Amand T.S., Zhang M., Ramamurthy R., Qiu M., Chen Y. Msx1 is required for the induction of Patched by Sonic hedgehog in the mammalian tooth germ. Dev. Dyn. 1999, 215:45-53.
65. Zhang Z., Lan Y., Chai Y., Jiang R. Antagonistic actions of Msx1 and Osr2 pattern mammalian teeth into a single row. Science 2009, 323:1232-1234.
66. Zhang Z., Song Y., Zhao X., Zhang X., Fermin C., Chen Y. Rescue of cleft palate in Msx1-deficient mice by transgenic Bmp4 reveals a network of BMP and Shh signaling in the regulation of mammalian palatogenesis. Development 2002, 129:4135-4146.
67. Zhang Z., Yu X., Zhang Y., Geronimo B., Lovelie A., Fromm S.H., Chen Y.P. Targeted misexpression of constitutively active BMP receptor-IB causes bifurcation, duplication, and posterior transformation of digit in mouse limb. Dev. Biol. 2000, 220:154-167.
68. Zuniga E., Rippen M., Alexander C., Schilling T.F., Crump J.G. Gremlin 2 regulates distinct roles of BMP and Endothelin 1 signaling in dorsoventral patterning of the facial skeleton. Development 2011, 138:5147-5156.