Maternal Interferon Regulatory Factor 6 is required for the differentiation of primary superficial epithelia in Danio and Xenopus embryos

Developmental Biology

Volumn 325, Issue 1, 2009, Pages 249-262

  Sabel, Jaime L ^a   d'Alençon, Claudia ^b   O'Brien, Erin K ^c   Otterloo, Eric Van ^a   Lutz, Katie ^a   Cuykendall, Tawny N ^d   Schutte, Brian C ^a   Houston, Douglas W ^a,d   Cornell, Robert A ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

Enveloping layer; Epiboly; Gastrulation; Interferon Regulatory Factor 6; Keratin; Superficial epithelium; Trophectoderm

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; CELL ADHESION MOLECULE; INTERFERON REGULATORY FACTOR 6; PROTEIN EVL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTOMERE; BLASTULA; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; GASTRULATION; GENE DISRUPTION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC DISORDER; GENETIC TRANSCRIPTION; HISTOLOGY; MOUTH MUCOSA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA TRANSLATION; SKIN EPITHELIUM; XENOPUS LAEVIS; ZEBRA FISH;

ANIMALIA; DANIO; DANIO RERIO; XENOPUS LAEVIS;

EID: 57849091769     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.10.031     Document Type: Article

References (92)

1. Bailey C.M., Khalkhali-Ellis Z., Kondo S., Margaryan N.V., Seftor R.E., Wheaton W.W., et al. Mammary serine protease inhibitor (Maspin) binds directly to interferon regulatory factor 6: identification of a novel serpin partnership. J. Biol. Chem. 280 (2005) 34210-34217
2. Bailey C.M., Abbott D.E., Margaryan N.V., Khalkhali-Ellis Z., and Hendrix M.J. Interferon regulatory factor 6 promotes cell cycle arrest and is regulated by the proteasome in a cell cycle-dependent manner. Mol. Cell. Biol. 28 (2008) 2235-2243
3. Bailey C.M., Abbott D.E., Margaryan N.V., Khalkhali-Ellis Z., and Hendrix M.J. IRF6 promotes cell cycle arrest and is regulated by the proteasome in a cell cycle-dependent manner. Mol. Cell. Biol. 28 (2008) 2235-2243
4. Ben J., Jabs E.W., and Chong S.S. Genomic, cDNA and embryonic expression analysis of zebrafish IRF6, the gene mutated in the human oral clefting disorders Van der Woude and popliteal pterygium syndromes. Gene Expr. Patterns 5 (2005) 629-638
5. Betchaku T., and Trinkaus J.P. Contact relations, surface activity, and cortical microfilaments of marginal cells of the enveloping layer and of the yolk syncytial and yolk cytoplasmic layers of fundulus before and during epiboly. J. Exp. Zool. 206 (1978) 381-426
6. Bouvet J. Enveloping layer and periderm of the trout embryo (Salmo trutta fario L.)20U. Cell Tissue Res. 170 (1976) 367-382
7. Braissant O., and Wahli W. Differential expression of peroxisome proliferator-activated receptor-alpha, -beta, and -gamma during rat embryonic development. Endocrinology 139 (1998) 2748-2754
8. Bruce A.E., Howley C., Zhou Y., Vickers S.L., Silver L.M., King M.L., and Ho R.K. The maternally expressed zebrafish T-box gene eomesodermin regulates organizer formation. Development 130 (2003) 5503-5517
9. Butler K., Zorn A.M., and Gurdon J.B. Nonradioactive in situ hybridization to Xenopus tissue sections. Methods 23 (2001) 303-312
10. Chalmers A.D., Welchman D., and Papalopulu N. Intrinsic differences between the superficial and deep layers of the Xenopus ectoderm control primary neuronal differentiation. Dev. Cell 2 (2002) 171-182
11. Chalmers A.D., Strauss B., and Papalopulu N. Oriented cell divisions asymmetrically segregate aPKC and generate cell fate diversity in the early Xenopus embryo. Development 130 (2003) 2657-2668
12. Chalmers A.D., Pambos M., Mason J., Lang S., Wylie C., and Papalopulu N. aPKC, Crumbs3 and Lgl2 control apicobasal polarity in early vertebrate development. Development 132 (2005) 977-986
13. Chalmers A., Lachani K., Shin Y., Sherwood V., Cho K., and Papalopulu N. Grainyhead-like 3, a transcription factor identified in a microarray screen, promotes the specification of the superficial layer of the embryonic epidermis. Mech. Dev. 123 (2006) 702-718
14. Choi S.C., and Han J.K. Xenopus Cdc42 regulates convergent extension movements during gastrulation through Wnt/Ca2+ signaling pathway. Dev. Biol. 244 (2002) 342-357
15. Ciruna B., Weidinger G., Knaut H., Thisse B., Thisse C., Raz E., and Schier A.F. Production of maternal-zygotic mutant zebrafish by germ-line replacement. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 14919-14924
16. Cooper M.S., and D'Amico L.A. A cluster of noninvoluting endocytic cells at the margin of the zebrafish blastoderm marks the site of embryonic shield formation. Dev. Biol. 180 (1996) 184-198
17. Cornell R.A., and Eisen J.S. Delta signaling mediates segregation of neural crest and spinal sensory neurons from zebrafish lateral neural plate. Development 127 (2000) 2873-2882
18. D'Amico L.A., and Cooper M.S. Morphogenetic domains in the yolk syncytial layer of axiating zebrafish embryos. Dev. Dyn. 222 (2001) 611-624
19. Deblandre G.A., Wettstein D.A., Koyano-Nakagawa N., and Kintner C. A two-step mechanism generates the spacing pattern of the ciliated cells in the skin of Xenopus embryos. Development 126 (1999) 4715-4728
20. Detrich III H.W., Kieran M.W., Chan F.Y., Barone L.M., Yee K., Rundstadler J.A., et al. Intraembryonic hematopoietic cell migration during vertebrate development. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 10713-10717
21. Dollar G.L., Weber U., Mlodzik M., and Sokol S.Y. Regulation of Lethal giant larvae by Dishevelled. Nature 437 (2005) 1376-1380
22. Doyon Y., McCammon J.M., Miller J.C., Faraji F., Ngo C., Katibah G.E., et al. Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat. Biotechnol. 26 (2008) 702-708
23. Faure S., Cau J., de Santa Barbara P., Bigou S., Ge Q., Delsert C., and Morin N. Xenopus p21-activated kinase 5 regulates blastomeres' adhesive properties during convergent extension movements. Dev. Biol. 277 (2005) 472-492
24. Godsave S.F., Wylie C.C., Lane E.B., and Anderton B.H. Intermediate filaments in the Xenopus oocyte: the appearance and distribution of cytokeratin-containing filaments. J. Embryol. Exp. Morphol. 83 (1984) 157-167
25. Guttormsen J., Koster M.I., Stevens J.R., Roop D.R., Williams T., and Winger Q.A. Disruption of epidermal specific gene expression and delayed skin development in AP-2 gamma mutant mice. Dev. Biol. 317 (2008) 187-195
26. Hartenstein V. Early neurogenesis in Xenopus: the spatio-temporal pattern of proliferation and cell lineages in the embryonic spinal cord. Neuron 3 (1989) 399-411
27. Hatada S., Kinoshita M., Takahashi S., Nishihara R., Sakumoto H., Fukui A., et al. An interferon regulatory factor-related gene (xIRF-6) is expressed in the posterior mesoderm during the early development of Xenopus laevis. Gene 203 (1997) 183-188
28. Hayes J.M., Kim S.K., Abitua P.B., Park T.J., Herrington E.R., Kitayama A., et al. Identification of novel ciliogenesis factors using a new in vivo model for mucociliary epithelial development. Dev. Biol. 312 (2007) 115-130
29. Heasman J., Holwill S., and Wylie C.C. Fertilization of cultured Xenopus oocytes and use in studies of maternally inherited molecules. Methods Cell Biol. 36 (1991) 213-230
30. Helfrich I., Schmitz A., Zigrino P., Michels C., Haase I., le Bivic A., et al. Role of aPKC isoforms and their binding partners Par3 and Par6 in epidermal barrier formation. J. Invest. Dermatol. 127 (2007) 782-791
31. Hens M.D., Nikolic I., and Woolcock C.M. Regulation of Xenopus embryonic cell adhesion by the small GTPase, rac. Biochem. Biophys. Res. Commun. 298 (2002) 364-370
32. Hensey C., and Gautier J. A developmental timer that regulates apoptosis at the onset of gastrulation. Mech. Dev. 69 (1997) 183-195
33. Ho R.K. Cell movements and cell fate during zebrafish gastrulation. Dev. Suppl (1992) 65-73
34. Houston D.W., and King M.L. A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development 127 (2000) 447-456
35. Houston D.W., and Wylie C.W. Maternal Xenopus Zic2 negatively regulates Nodal-related gene expression during anteroposterior patterning. Development 127 (2005) 447-456
36. Hu Y., Baud V., Delhase M., Zhang P., Deerinck T., Ellisman M., et al. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase. Science 284 (1999) 316-320
37. Ikegami R., Hunter P., and Yager T.D. Developmental activation of the capability to undergo checkpoint-induced apoptosis in the early zebrafish embryo. Dev. Biol. 209 (1999) 409-433
38. Imboden M., Goblet C., Korn H., and Vriz S. Cytokeratin 8 is a suitable epidermal marker during zebrafish development. C. R. Acad. Sci., Ser. III 320 (1997) 689-700
39. Ingraham C.R., Kinoshita A., Kondo S., Yang B., Sajan S., Trout K.J., et al. Abnormal skin, limb and craniofacial morphogenesis in mice deficient for interferon regulatory factor 6 (Irf6). Nat. Genet. 38 (2006) 1335-1340
40. Johnson M.H., and McConnell J.M. Lineage allocation and cell polarity during mouse embryogenesis. Semin. Cell Dev. Biol. 15 (2004) 583-597
41. Jones E.A., and Woodland H.R. Development of the ectoderm in Xenopus: tissue specification and the role of cell association and division. Cell 44 (1986) 345-355
42. Kaji T., and Artinger K.B. dlx3b and dlx4b function in the development of Rohon-Beard sensory neurons and trigeminal placode in the zebrafish neurula. Dev. Biol. 276 (2004) 523-540
43. Kane D.A., Hammerschmidt M., Mullins M.C., Maischein H.M., Brand M., van Eeden F.J., et al. The zebrafish epiboly mutants. Development 123 (1996) 47-55
44. Kane D.A., McFarland K.N., and Warga R.M. Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly. Development 132 (2005) 1105-1116
45. Keller R.E. The cellular basis of epiboly: an SEM study of deep cell rearrangement during gastrulation in Xenopus laevis. J. Embryol. Exp. Morphol. 60 (1980) 201-234
46. Keller R.E., and Trinkaus J.P. Rearrangement of enveloping layer cells without disruption of the epithelial permeability barrier as a factor in Fundulus epiboly. Dev. Biol. 120 (1987) 12-24
47. Kimmel C.B., Warga R.M., and Schilling T.F. Origin and organization of the zebrafish fate map. Development 108 (1990) 581-594
48. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., and Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995) 253-310
49. Kimmel C.B., Miller C.T., Kruze G., Ullmann B., BreMiller R.A., Larison K.D., and Snyder H.C. The shaping of pharyngeal cartilages during early development of the zebrafish. Dev. Biol. 203 (1998) 245-263
50. Klein S.L., Strausberg R.L., Wagner L., Pontius J., Clifton S.W., and Richardson P. Genetic and genomic tools for Xenopus research: the NIH Xenopus initiative. Dev. Dyn. 225 (2002) 384-391
51. Knight A.S., Schutte B.C., Jiang R., and Dixon M.J. Developmental expression analysis of the mouse and chick orthologues of IRF6: the gene mutated in Van der Woude syndrome. Dev. Dyn. 235 (2006) 1441-1447
52. Kondo S., Schutte B.C., Richardson R.J., Bjork B.C., Knight A.S., Watanabe Y., et al. Mutations in IRF6 cause Van der Woude and popliteal pterygium syndromes. Nat. Genet. 32 (2002) 285-289
53. Kondo S., Schutte B.C., Richardson R.J., Bjork B.C., Knight A.S., Watanabe Y., et al. Mutations in IRF6 cause Van der Woude and popliteal pterygium syndromes. Nat. Genet. 32 (2002) 285-289
54. Koppen M., Fernandez B.G., Carvalho L., Jacinto A., and Heisenberg C.P. Coordinated cell-shape changes control epithelial movement in zebrafish and Drosophila. Development 133 (2006) 2671-2681
55. Lane E.B., Bártek J., Purkis P.E., and Leigh I.M. Keratin antigens in differentiating skin. Ann. N. Y. Acad. Sci. 455 (1985) 241-258
56. Li W., and Cornell R.A. Redundant activities of Tfap2a and Tfap2c are required for neural crest induction and development of other non-neural ectoderm derivatives in zebrafish embryos. Dev. Biol. 304 (2007) 338-354
57. Li Q., Lu Q., Hwang J.Y., Buscher D., Lee K.F., Izpisua-Belmonte J.C., and Verma I.M. IKK1-deficient mice exhibit abnormal development of skin and skeleton. Genes Dev. 13 (1999) 1322-1328
58. Li Q., Lu Q., Estepa G., and Verma I.M. Identification of 14-3-3sigma mutation causing cutaneous abnormality in repeated-epilation mutant mouse. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 15977-15982
59. Lyons S.E., Shue B.C., Lei L., Oates A.C., Zon L.I., and Liu P.P. Molecular cloning, genetic mapping, and expression analysis of four zebrafish c/ebp genes. Gene 281 (2001) 43-51
60. Mathavan S., Lee S.G., Mak A., Miller L.D., Murthy K.R., Govindarajan K.R., et al. Transcriptome analysis of zebrafish embryogenesis using microarrays. PLoS Genet. 1 (2005) 260-276
61. McFarland K.N., Warga R.M., and Kane D.A. Genetic locus half baked is necessary for morphogenesis of the ectoderm. Dev. Dyn. 233 (2005) 390-406
62. Meng X., Noyes M.B., Zhu L.J., Lawson N.D., and Wolfe S.A. Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat. Biotechnol. 26 (2008) 695-701
63. Nagafuchi A. Molecular architecture of adherens junctions. Curr. Opin. Cell Biol. 13 (2001) 600-603
64. Nakaya M., Fukui A., Izumi Y., Akimoto K., Asashima M., and Ohno S. Meiotic maturation induces animal-vegetal asymmetric distribution of aPKC and ASIP/PAR-3 in Xenopus oocytes. Development 127 (2000) 5021-5031
65. Nasevicius, A., and Ekker, S.C. 2000. Effective targeted gene 'knockdown' in zebrafish. Nat Genet 26, 216-20. taf/DynaPage.taf?file=/ng/journal/v26/n2/full/ng1000_216.html taf/DynaPage.taf?file=/ng/journal/v26/n2/abs/ng1000_216.html.
66. Nieuwkoop P., and Faber J. Normal Tables of Xenopus laevis (1956), New Holland Publishing Co, Amsterdam
67. O'Brien E.K., d'Alencon C., Bonde G., Li W., Schoenebeck J., Allende M.L., et al. Transcription factor Ap-2alpha is necessary for development of embryonic melanophores, autonomic neurons and pharyngeal skeleton in zebrafish. Dev. Biol. 265 (2004) 246-261
68. Ossipova O., Tabler J., Green J., and Sokol S. PAR1 specifies ciliated cells in vertebrate ectoderm downstream of aPKC. Development 134 (2007) 4297-4306
69. Oteiza P., Koppen M., Concha M.L., and Heisenberg C.P. Origin and shaping of the laterality organ in zebrafish. Development 135 (2008) 2807-2813
70. Paun A., and Pitha P.M. The IRF family, revisited. Biochimie 89 (2007) 744-753
71. Pei W., Noushmehr H., Costa J., Ouspenskaia M.V., Elkahloun A.G., and Feldman B. An early requirement for maternal FoxH1 during zebrafish gastrulation. Dev. Biol. 310 (2007) 10-22
72. Postlethwait J.H., Yan Y.L., Gates M.A., Horne S., Amores A., Brownlie A., et al. Vertebrate genome evolution and the zebrafish gene map. Nat. Genet. 18 (1998) 345-349
73. Regen C.M., and Steinhardt R.A. Global properties of the Xenopus blastula are mediated by a high-resistance epithelial seal. Dev. Biol. 113 (1986) 147-154
74. Richardson R.J., Dixon J., Malhotra S., Hardman M.J., Knowles L., Boot-Handford R.P., et al. Irf6 is a key determinant of the keratinocyte proliferation-differentiation switch. Nat. Genet. 38 (2006) 1329-1334
75. Sagerstrom C.G., Gammill L.S., Veale R., and Sive H. Specification of the enveloping layer and lack of autoneuralization in zebrafish embryonic explants. Dev. Dyn. 232 (2005) 85-97
76. Schulte-Merker S., van Eeden F.J., Halpern M.E., Kimmel C.B., and Nusslein-Volhard C. no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. Development 120 (1994) 1009-1015
77. Sive H., Grainger R.M., and Harland R.M. Early Development of Xenopus laevis: a Laboratory Manual (2000), Cold Spring Harbor Laboratory Press, New York
78. Solnica-Krezel L. Gastrulation in zebrafish - all just about adhesion?. Curr. Opin. Genet. Dev. 16 (2006) 433-441
79. Solnica-Krezel L., and Driever W. Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly. Development 120 (1994) 2443-2455
80. Strahle U., and Jesuthasan S. Ultraviolet irradiation impairs epiboly in zebrafish embryos: evidence for a microtubule-dependent mechanism of epiboly. Development 119 (1993) 909-919
81. Suzuki A., and Ohno S. The PAR-aPKC system: lessons in polarity. J. Cell Sci. (2006) 979-987
82. Taniguchi T., Ogasawara K., Takaoka A., and Tanaka N. IRF family of transcription factors as regulators of host defense. Annu. Rev. Immunol. 19 (2001) 623-655
83. Torpey N., Wylie C.C., and Heasman J. Function of maternal cytokeratin in Xenopus development. Nature 357 (1992) 413-415
84. Truong A.B., and Khavari P.A. Control of keratinocyte proliferation and differentiation by p63. Cell. Cycle 6 (2007) 295-299
85. Uribe, R., Jay, D., in press. A review of actin binding proteins: new perspectives. Mol. Biol. Rep. doi:10.1007/s11033-007-9159-2.
86. Wagner D., Dosch R., Mintzer K., Wiemelt A., and Mullins M. Maternal control of development at the midblastula transition and beyond: mutants from the zebrafish II. Dev. Cell 6 (2004) 781-790
87. Wang X., Bolotin D., Chu D.H., Polak L., Williams T., and Fuchs E. AP-2alpha: a regulator of EGF receptor signaling and proliferation in skin epidermis. J. Cell Biol. 172 (2006) 409-421
88. Warga R.M., and Kimmel C.B. Cell movements during epiboly and gastrulation in zebrafish. Development 108 (1990) 569-580
89. Westerfield M. The Zebrafish Book (1993), University of Oregon Press, Eugene, OR
90. Wunnenberg-Stapleton K., Blitz I.L., Hashimoto C., and Cho K.W. Involvement of the small GTPases XRhoA and XRnd1 in cell adhesion and head formation in early Xenopus development. Development 126 (1999) 5339-5351
91. Zalik S.E., Lewandowski E., Kam Z., and Geiger B. Cell adhesion and the actin cytoskeleton of the enveloping layer in the zebrafish embryo during epiboly. Biochem. Cell. Biol. 77 (1999) 527-542
92. Zucchero T.M., Cooper M.E., Maher B.S., Daack-Hirsch S., Nepomuceno B., Ribeiro L., et al. Interferon regulatory factor 6 (IRF6) gene variants and the risk of isolated cleft lip or palate. N. Engl. J. Med. 351 (2004) 769-780