Foxi transcription factors promote pharyngeal arch development by regulating formation of FGF signaling centers

Developmental Biology

Volumn 390, Issue 1, 2014, Pages 1-13

  Edlund, Renée K ^a   Ohyama, Takahiro ^b,d   Kantarci, Husniye ^c   Riley, Bruce B ^c   Groves, Andrew K ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b HOUSE RESEARCH INSTITUTE   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Craniofacial development; FGF; Neural Crest; Pharyngeal arch

Indexed keywords

FIBROBLAST GROWTH FACTOR 3; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTOR; FORKHEAD TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXI; TRANSCRIPTION FACTOR FOXI1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRANCHIAL ARCH; CELL DEATH; CELL DIFFERENTIATION; CONTROLLED STUDY; DEVELOPMENTAL GENE; ECTODERM; EMBRYO; ENDODERM; FGF3 GENE; FGF8 GENE; FOXI1 GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; MOUSE; NEURAL CREST CELL; NONHUMAN; ORGANOGENESIS; PHARYNGEAL ARCH DEVELOPMENT; PHARYNX; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ZEBRA FISH; CELL MIGRATION; CELL SURVIVAL; CRANIOFACIAL DEVELOPMENT; EMBRYO PATTERN FORMATION; EXTERNAL EAR MALFORMATION; FACIAL BONE; HEAT SHOCK; INNER EAR MALFORMATION; MANDIBLE; MIDDLE EAR MALFORMATION; NERVE CELL DIFFERENTIATION; SKULL DEFECT;

DANIO RERIO; MUS; VERTEBRATA;

CRANIOFACIAL DEVELOPMENT; FGF; NEURAL CREST; PHARYNGEAL ARCH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BODY PATTERNING; BRANCHIAL REGION; CELL MOVEMENT; ECTODERM; EMBRYO, MAMMALIAN; EMBRYO, NONMAMMALIAN; ENDODERM; FIBROBLAST GROWTH FACTOR 3; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTORS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; IN SITU HYBRIDIZATION; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; NEURAL CREST; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84897570316     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.03.004     Document Type: Article

References (50)

1. Abu-Issa R., Smyth G., Smoak I., Yamamura K., Meyers E.N. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 2002, 129:4613-4625.
2. Adams D.J., Quail M.A., Cox T., van der Weyden L., Gorick B.D., Su Q., Chan W.I., Davies R., Bonfield J.K., Law F., Humphray S., Plumb B., Liu P., Rogers J., Bradley A. A genome-wide, end-sequenced 129Sv BAC library resource for targeting vector construction. Genomics 2005, 86:753-758.
3. Beermann F., Kaloulis K., Hofmann D., Murisier F., Bucher P., Trumpp A. Identification of evolutionarily conserved regulatory elements in the mouse Fgf8 locus. Genesis 2006, 44:1-6.
4. Brewer S., Jiang X., Donaldson S., Williams T., Sucov H.M. Requirement for AP-2alpha in cardiac outflow tract morphogenesis. Mech. Dev. 2002, 110:139-149.
5. Brito J.M., Teillet M.A., Le Douarin N.M. An early role for sonic hedgehog from foregut endoderm in jaw development: ensuring neural crest cell survival. Proc. Natl. Acad. Sci. USA 2006, 103:11607-11612.
6. Cobourne M.T., Sharpe P.T. Tooth and jaw: molecular mechanisms of patterning in the first branchial arch. Arch. Oral Biol. 2003, 48:1-14.
7. Couly G., Creuzet S., Bennaceur S., Vincent C., Le Douarin N.M. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 2002, 129:1061-1073.
8. Crossley P.H., Martin G.R. The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 1995, 121:439-451.
9. Crump J.G., Maves L., Lawson N.D., Weinstein B.M., Kimmel C.B. An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 2004, 131:5703-5716.
10. Danesh S.M., Villasenor A., Chong D., Soukup C., Cleaver O. BMP and BMP receptor expression during murine organogenesis. Gene Expr. Patterns 2009, 9:255-265.
11. David N.B., Saint-Etienne L., Tsang M., Schilling T.F., Rosa F.M. Requirement for endoderm and FGF3 in ventral head skeleton formation. Development 2002, 129:4457-4468.
12. 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.
13. Drogemuller C., Karlsson E.K., Hytonen M.K., Perloski M., Dolf G., Sainio K., Lohi H., Lindblad-Toh K., Leeb T. A mutation in hairless dogs implicates FOXI3 in ectodermal development. Science 2008, 321:1462.
14. Grigoriou M., Tucker A.S., Sharpe P.T., Pachnis V. Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeodomain encoding genes, suggests a role in mammalian head development. Development 1998, 125:2063-2074.
15. Haworth K.E., Healy C., Morgan P., Sharpe P.T. Regionalisation of early head ectoderm is regulated by endoderm and prepatterns the orofacial epithelium. Development 2004, 131:4797-4806.
16. Haworth K.E., Wilson J.M., Grevellec A., Cobourne M.T., Healy C., Helms J.A., Sharpe P.T., Tucker A.S. Sonic hedgehog in the pharyngeal endoderm controls arch pattern via regulation of Fgf8 in head ectoderm. Dev. Biol. 2007, 303:244-258.
17. Hulander M., Kiernan A.E., Blomqvist S.R., Carlsson P., Samuelsson E.J., Johansson B.R., Steel K.P., Enerback S. Lack of pendrin expression leads to deafness and expansion of the endolymphatic compartment in inner ears of Foxi1 null mutant mice. Development 2003, 130:2013-2025.
18. Hulander M., Wurst W., Carlsson P., Enerback S. The winged helix transcription factor Fkh10 is required for normal development of the inner ear. Nat. Genet. 1998, 20:374-376.
19. Khatri S.B., Groves A.K. Expression of the Foxi2 and Foxi3 transcription factors during development of chicken sensory placodes and pharyngeal arches. Gene Expr. Patterns 2013, 13:38-42.
20. Komisarczuk A.Z., Kawakami K., Becker T.S. Cis-regulation and chromosomal rearrangement of the fgf8 locus after the teleost/tetrapod split. Dev. Biol. 2009, 336:301-312.
21. Liu W., Selever J., Murali D., Sun X., Brugger S.M., Ma L., Schwartz R.J., Maxson R., Furuta Y., Martin J.F. Threshold-specific requirements for Bmp4 in mandibular development. Dev. Biol. 2005, 283:282-293.
22. Lumsden A., Sprawson N., Graham A. Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 1991, 113:1281-1291.
23. Maemura K., Kurihara H., Kurihara Y., Oda H., Ishikawa T., Copeland N.G., Gilbert D.J., Jenkins N.A., Yazaki Y. Sequence analysis, chromosomal location, and developmental expression of the mouse preproendothelin-1 gene. Genomics 1996, 31:177-184.
24. Marinic M., Aktas T., Ruf S., Spitz F. An integrated holo-enhancer unit defines tissue and gene specificity of the Fgf8 regulatory landscape. Dev. Cell 2013, 24:530-542.
25. Medeiros D.M., Crump J.G. New perspectives on pharyngeal dorsoventral patterning in development and evolution of the vertebrate jaw. Dev. Biol. 2012, 371:121-135.
26. Meyers E.N., Lewandoski M., Martin G.R. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 1998, 18:136-141.
27. Millimaki B.B., Sweet E.M., Riley B.B. Sox2 is required for maintenance and regeneration, but not initial development, of hair cells in the zebrafish inner ear. Dev. Biol. 2010, 338:262-269.
28. Minoux M., Rijli F.M. Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development 2010, 137:2605-2621.
29. Neubuser A., Koseki H., Balling R. Characterization and developmental expression of Pax9, a paired-box-containing gene related to Pax1. Dev. Biol. 1995, 170:701-716.
30. Nissen R.M., Yan J., Amsterdam A., Hopkins N., Burgess S.M. Zebrafish foxi one modulates cellular responses to Fgf signaling required for the integrity of ear and jaw patterning. Development 2003, 130:2543-2554.
31. Noden D.M., Trainor P.A. Relations and interactions between cranial mesoderm and neural crest populations. J. Anat. 2005, 207:575-601.
32. Ohyama T., Groves A.K. Expression of mouse Foxi class genes in early craniofacial development. Dev. Dyn.: Off. Publ. Am. Assoc. Anat. 2004, 231:640-646.
33. Ovchinnikov, D., 2009. Alcian Blue/Alizarin Red Staining of Cartilage and Bone in Mouse. Cold Spring Harbor Protocols 2009, pdb prot5170.
34. Passos-Bueno M.R., Ornelas C.C., Fanganiello R.D. Syndromes of the first and second pharyngeal arches: a review. Am. J. Med. Genet. Part A 2009, 149A:1853-1859.
35. Phillips B.T., Bolding K., Riley B.B. Zebrafish fgf3 and fgf8 encode redundant functions required for otic placode induction. Dev. Biol. 2001, 235:351-365.
36. Qiu M., Bulfone A., Ghattas I., Meneses J.J., Christensen L., Sharpe P.T., Presley R., Pedersen R.A., Rubenstein J.L. Role of the Dlx homeobox genes in proximodistal patterning of the branchial arches: mutations of Dlx-1, Dlx-2, and Dlx-1 and -2 alter morphogenesis of proximal skeletal and soft tissue structures derived from the first and second arches. Dev. Biol. 1997, 185:165-184.
37. Sandell L.L., Kurosaka H., Trainor P.A. Whole mount nuclear fluorescent imaging: convenient documentation of embryo morphology. Genesis 2012, 50:844-850.
38. Schilling T.F., Kimmel C.B. Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 1994, 120:483-494.
39. Serbedzija G.N., Bronner-Fraser M., Fraser S.E. Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 1992, 116:297-307.
40. Solomon K.S., Kudoh T., Dawid I.B., Fritz A. Zebrafish foxi1 mediates otic placode formation and jaw development. Development 2003, 130:929-940.
41. Solomon K.S., Logsdon J.M., Fritz A. Expression and phylogenetic analyses of three zebrafish FoxI class genes. Dev. Dyn.: Off. Publ. Am. Assoc. Anat. 2003, 228:301-307.
42. Stern C.D. Detection of multiple gene products simultaneously by in situ hybridization and immunohistochemistry in whole mounts of avian embryos. Curr. Top. Dev. Biol. 1998, 36:223-243.
43. Sweet E.M., Vemaraju S., Riley B.B. Sox2 and Fgf interact with Atoh1 to promote sensory competence throughout the zebrafish inner ear. Dev. Biol. 2011, 358:113-121.
44. Szabo-Rogers H.L., Smithers L.E., Yakob W., Liu K.J. New directions in craniofacial morphogenesis. Dev. Biol. 2010, 341:84-94.
45. Trainor P.A., Krumlauf R. Patterning the cranial neural crest: hindbrain segmentation and Hox gene plasticity. Nat. Rev. Neurosci. 2000, 1:116-124.
46. Trumpp A., Depew M.J., Rubenstein J.L., Bishop J.M., Martin G.R. Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev. 1999, 13:3136-3148.
47. Tucker A.S., Yamada G., Grigoriou M., Pachnis V., Sharpe P.T. Fgf-8 determines rostral-caudal polarity in the first branchial arch. Development 1999, 126:51-61.
48. Vemaraju S., Kantarci H., Padanad M.S., Riley B.B. A spatial and temporal gradient of Fgf differentially regulates distinct stages of neural development in the zebrafish inner ear. PLoS Genet. 2012, 8:e1003068.
49. Warming S., Costantino N., Court D.L., Jenkins N.A., Copeland N.G. Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res. 2005, 33:e36.
50. Zeng J., Yan J., Wang T., Mosbrook-Davis D., Dolan K.T., Christensen R., Stormo G.D., Haussler D., Lathrop R.H., Brachmann R.K., Burgess S.M. Genome wide screens in yeast to identify potential binding sites and target genes of DNA-binding proteins. Nucleic Acids Res. 2008, 36:e8.