Dickkopf1 Is Required for Embryonic Head Induction and Limb Morphogenesis in the Mouse

Developmental Cell

Volumn 1, Issue 3, 2001, Pages 423-434

  Mukhopadhyay, Mahua ^a   Shtrom, Svetlana ^a   Rodriguez Esteban, Concepcion ^b   Chen, Lan ^a   Tsukui, Tohru ^b   Gomer, Lauren ^a   Dorward, David W ^c   Glinka, Andrei ^d   Grinberg, Alexander ^a   Huang, Sing Ping ^a   Niehrs, Christof ^d   Belmonte, Juan Carlos Izpisúa ^b   Westphal, Heiner ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; BONE MORPHOGENETIC PROTEIN; DKK1 PROTEIN, MOUSE; DKK1 PROTEIN, ZEBRAFISH; ONCOPROTEIN; PROTEIN; SIGNAL PEPTIDE; WNT PROTEIN; ZEBRAFISH PROTEIN;

ANIMAL; ARTICLE; BRAIN; CHICK EMBRYO; DRUG ANTAGONISM; EMBRYO; EMBRYO INDUCTION; GENE TARGETING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAD; IN SITU HYBRIDIZATION; LIMB; METABOLISM; MOLECULAR GENETICS; MORPHOGENESIS; MOUSE; PHYSIOLOGY; PRENATAL DEVELOPMENT; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ANIMALS; BIOLOGICAL MARKERS; BONE MORPHOGENETIC PROTEINS; BRAIN; CHICK EMBRYO; EMBRYO; EMBRYONIC INDUCTION; EXTREMITIES; GENE TARGETING; HEAD; IN SITU HYBRIDIZATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; PROTEINS; PROTO-ONCOGENE PROTEINS; WNT PROTEINS; ZEBRAFISH PROTEINS;

EID: 18044399916     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1534-5807(01)00041-7     Document Type: Article

References (86)

1. -/- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development. 121:1995;3279-3290.
2. Ang S.L., Conlon R.A., Jin O., Rossant J. Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants. Development. 120:1994;2979-2989.
3. Ang S.L., Jin O., Rhinn M., Daigle N., Stevenson L., Rossant J. A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development. 122:1996;243-252.
4. Bachiller D., Klingensmith J., Kemp C., Belo J.A., Anderson R.M., May S.R., McMahon J.A., McMahon A.P., Harland R.M., Rossant J., De Robertis E.M. The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature. 403:2000;658-661.
5. Beddington R.S., Robertson E.J. An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development. 105:1989;733-737.
6. Beddington R.S., Robertson E.J. Anterior patterning in mouse. Trends Genet. 14:1998;277-284.
7. Belo J.A., Bachiller D., Agius E., Kemp C., Borges A.C., Marques S., Piccolo S., De Robertis E.M. Cerberus-like is a secreted BMP and nodal antagonist not essential for mouse development. Genesis. 26:2000;265-270.
8. Bendall A.J., Abate-Shen C. Roles for Msx and Dlx homeoproteins in vertebrate development. Gene. 247:2000;17-31.
9. Bhanot P., Brink M., Harryman Samos C., Hsieh J.-C., Wang Y., Macke J.P., Andrew D., Nathans J., Nusse R. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature. 382:1996;225-230.
10. Borello U., Coletta M., Tajbakhsh S., Leyns L., De Robertis E.M., Buckingham M., Cossu G. Transplacental delivery of the Wnt antagonist Frzb1 inhibits development of caudal paraxial mesoderm and skeletal myogenesis in mouse embryos. Development. 126:1999;4247-4255.
11. Bradley L., Wainstock D., Sive H. Positive and negative signals modulate formation of the Xenopus cement gland. Development. 122:1996;2739-2750.
12. Cadigan K.M., Nusse R.M. Wnt signaling. a common theme in animal development Genes Dev. 11:1997;3286-3305.
13. Camus A., Tam P.P. The organizer of the gastrulating mouse embryo. Curr. Top. Dev. Biol. 45:1999;117-153.
14. Capdevila J., Tsukui T., Rodriguez-Esteban C., Zappavigna V., Izpisúa Belmonte J.C. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mol. Cell. 4:1999;839-849.
15. Chen Y., Zhao X. Shaping limbs by apoptosis. J. Exp. Zool. 282:1998;691-702.
16. Christian J.L., Moon R.T. Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus. Genes Dev. 7:1993;13-28.
17. Dattani M.T., Martinez-Barbera J.P., Thomas P.Q., Brickman J.M., Gupta R., Martensson I.L., Toresson H., Fox M., Wales J.K., Hindmarsh P.C.et al. Mutations in the homeobox gene HESX1/Hesx1 associated with septo-optic dysplasia in human and mouse. Nat. Genet. 19:1998;125-133.
18. Echelard Y., Epstein D.J., St-Jacques B., Shen L., Mohler J., McMahon J.A., McMahon A.P. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell. 75:1993;1417-1430.
19. Ellies D.L., Church V., Francis-West P., Lumsden A. The WNT antagonist cSFRP2 modulates programmed cell death in the developing hindbrain. Development. 127:2000;5285-5295.
20. Foley A.C., Skromne I., Stern C.D. Reconciling different models of forebrain induction and patterning. a dual role for the hypoblast Development. 127:2000;3839-3854.
21. Gañán Y., Macias D., Duterque-Coquillaud M., Ros M., Hurle J. Role of TGFBs and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development. 122:1996;2349-2357.
22. Gañán Y., Macias D., Basco R.D., Merino R., Hurle J.M. Morphological diversity of the avian foot is related with the pattern of Msx gene expression in the developing autopod. Dev. Biol. 196:1998;33-41.
23. Glinka A., Wu W., Onichtchouk D., Blumenstock C., Niehrs C. Head induction by simultaneous repression of BMP and Wnt signalling in Xenopus. Nature. 389:1997;517-519.
24. Glinka A., Wu W., Delius H., Monaghan P.A., Blumenstock C., Niehrs C. Dickkopf1 is a member of a new family of secreted proteins and functions in head induction. Nature. 391:1998;357-362.
25. Grotewold L., Theil T., Rüther U. Expression pattern of DKK1 during mouse limb development. Mech. Dev. 89:1999;151-153.
26. Hashimoto H., Itoh M., Yamanaka Y., Yamashita S., Shimizu T., Solnica-Krezel L., Hibi M., Hirano T. Zebrafish DKK1 functions in forebrain specification and axial mesendoderm formation. Dev. Biol. 217:2000;138-152.
27. Hermesz E., Mackem S., Mohan K.A. Rpx. a novel anterior-restricted homeobox gene progressively activated in the prechordal plate, anterior neural plate and Rathke's pouch of the mouse embryo Development. 122:1996;41-52.
28. Herrmann B.G. Action of the Brachyury gene in mouse embryogenesis. Ciba Found. Symp. 165:1992;78-86.
29. Hogan B., Beddington R., Costantini F., Lacy E. Isolating extraembryonic membranes. In Manipulating the Mouse Embryo. A Laboratory Manual. 1994;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. pp. 160-162.
30. Hoppler S., Brown J.D., Moon R.T. Expression of a dominant-negative wnt blocks induction of MyoD in Xenopus embryos. Genes Dev. 10:1996;2805-2817.
31. Hsieh J.C., Kodjabachian L., Rebbert M.L., Rattner A., Smallwood P.M., Samos C.H., Nusse R., Dawid I.B., Nathans J. A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature. 398:1999;431-436.
32. Huelsken J., Vogel R., Brinkmann V., Erdmann B., Birchmeier C., Birchmeier W. Requirement for β-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148:2000;567-578.
33. Joyner A.L., Martin G.R. En-1 and En-2, two mouse genes with sequence homology to the Drosophila engrailed gene. expression during embryogenesis Genes Dev. 1:1987;29-38.
34. Katagiri T., Boorla S., Frendo J.L., Hogan B.L., Karsenty G. Skeletal abnormalities in doubly heterozygous Bmp4 and Bmp7 mice. Dev. Genet. 22:1998;340-348.
35. Kawakami Y., Capdevila J., Buscher D., Itoh T., Esteban C.R., Belmonte J.C. Wnt signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell. 104:2001;891-900.
36. Kazanskaya O., Glinka A., Niehrs C. The role of Xenopus Dickkopf1 in prechordal plate specification and neural patterning. Development. 127:2000;4981-4992.
37. Kengaku M., Capdevila J., Rodriguez-Esteban C., De La Peña J., Johnson R.L., Belmonte J.C., Tabin C.J. Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science. 280:1998;1274-1277.
38. Kim C.H., Oda T., Itoh M., Jiang D., Artinger K.B., Chandrasekharappa S.C., Driever W., Chitnis A.B. Repressor activity of Headless/Tcf3 is essential for vertebrate head formation. Nature. 407:2000;913-916.
39. Krupnik V.E., Sharp J.D., Jiang C., Robison K., Chickering T.W., Amaravadi L., Brown D.E., Guyot D., Mays G., Leiby K.et al. Functional and structural diversity of the human Dickkopf gene family. Gene. 238:1999;301-313.
40. Lewandoski M., Sun X., Martin G.R. Fgf8 signalling from the AER is essential for normal limb development. Nat. Genet. 26:2000;460-463.
41. Leyns L., Bouwmeester T., Kim S.-H., Piccolo S., De Robertis E.M. Frzb-1 is a secreted antagonist of wnt-signals expressed in the Spemann organizer. Cell. 88:1997;747-756.
42. Liu P., Wakamiya M., Shea M.J., Albrecht U., Behringer R.R., Bradley A. Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22:1999;361-365.
43. Lowe L.A., Kuehn M.R. Whole mount in-situ hybridization to study gene expression during mouse development. Methods Mol. Biol. 137:2000;125-137.
44. Luo G., Hofmann C., Bronckers A.L., Sohocki M., Bradley A., Karsenty G. BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev. 9:1995;2808-2820.
45. Mao B., Wu W., Li Y., Hoppe D., Stannek P., Glinka A., Niehrs C. LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature. 411:2001;321-325.
46. Martinez-Barbera J.P., Rodriguez T.A., Beddington R.S. The homeobox gene Hesx1 is required in the anterior neural ectoderm for normal forebrain formation. Dev. Biol. 223:2000;422-430.
47. Marvin M.J., Di Rocco G., Gardiner A., Bush S.M., Lassar A.B. Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes Dev. 15:2001;316-327.
48. Matsuo I., Kuratani S., Kimura C., Takeda N., Aizawa S. Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 9:1995;2646-2658.
49. McGrew L.L., Hoppler S., Moon R.T. Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus. Mech. Dev. 69:1997;105-114.
50. Miyake S., Makimura M., Kanegae Y., Harada S., Sato Y., Takamori K., Tokuda C., Saito I. Efficient generation of recombinant adenoviruses using adenovirus DNA-terminal protein complex and a cosmid bearing the full-length virus genome. Proc. Natl. Acad. Sci. USA. 93:1996;1320-1324.
51. Monaghan A.P., Kioschis P., Wu W., Zuniga A., Bock D., Poustka A., Delius H., Niehrs C. Dickkopf genes are co-ordinately expressed in mesodermal lineages. Mech. Dev. 87:1999;45-56.
52. Moon A.M., Capecchi M.R. Fgf8 is required for outgrowth and patterning of the limbs. Nat. Genet. 26:2000;455-459.
53. Moon R.T., Brown J.D., Torres M. Wnts modulate cell fate and behavior during vertebrate development. Trends Genet. 13:1997;157-162. a.
54. Moon R.T., Brown J.D., Yang-Snyder J.A., Miller J.R. Structurally related receptors and antagonists compete for secreted Wnt ligands. Cell. 88:1997;725-728. b.
55. Nagy A., Rossant J., Nagy R., Abramow-Newerly W., Roder J.C. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA. 90:1993;8424-8428.
56. Niehrs C. Head in the WNT. the molecular nature of Spemann's head organizer Trends Genet. 15:1999;314-319.
57. Oliver G., Mailhos A., Wehr R., Copeland N.G., Jenkins N.A., Gruss P. Six3, a murine homologue of the Sine Oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development. 121:1995;4045-4055.
58. Pearce J.J., Penny G., Rossant J. A mouse Cerberus/Dan-related gene family. Dev. Biol. 209:1999;98-110.
59. Perea-Gomez A., Lawson K.A., Rhinn M., Zakin L., Brulet P., Mazan S., Ang S.L. Otx2 is required for visceral endoderm movement and for the restriction of posterior signals in the epiblast of the mouse embryo. Development. 128:2001;753-765.
60. Piccolo S., Agius E., Leyns L., Bhattacharya S., Grunz H., Bouwmeester T., De Robertis E.M. The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature. 397:1999;707-710.
61. Pöpperl H., Schmidt C., Wilson V., Hume C.R., Dodd J., Krumlauf R., Beddington R.S.P. Misexpression of Cwnt8c in the mouse induces an ectopic embryonic axis and causes a truncation of the anterior neuroectoderm. Development. 124:1997;2997-3005.
62. Rattner A., Hsieh J.-C., Smallwood P.M., Gilbert D., Copeland N.G., Jenkins N.A., Nathans J. A family of secreted proteins contains homology to the cysteine-rich ligand binding domain of frizzled receptors. Proc. Natl. Acad. Sci. USA. 94:1997;2859-2863.
63. Robinson G.W., Wray S., Mahon K.A. Spatially restricted expression of a member of a new family of murine Distal-less homeobox genes in the developing forebrain. New Biol. 3:1991;1183-1194.
64. Rodriguez-Esteban C., Schwabe J.W.R., De La Peña J., Foys B., Eshelman B., Izpisúa Belmonte J.C. Radical fringe positions the apical ectodermal ridge at the dorsoventral boundary of the vertebrate limb. Nature. 386:1997;360-366.
65. Saga Y., Hata N., Kobayashi S., Magnuson T., Seldin M., Taketo M.M. MesP1. a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation Development. 122:1996;2769-2778.
66. Schneider V.A., Mercola M. Spatially distinct head and heart inducers within the Xenopus organizer region. Curr. Biol. 9:1999;800-809.
67. Schneider V.A., Mercola M. Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev. 15:2001;304-315.
68. Semënov M.V., Tamai K., Brott B.K., Kuhl M., Sokol S., He X. Head inducer Dickkopf-1 is a ligand for Wnt co-receptor LRP6. Curr. Biol. 11:2001;951-961.
69. Shawlot W., Wakamiya M., Kwan K.M., Kania A., Jessell T.M., Behringer R.R. Lim1 is required in both primitive streak-derived tissues and visceral endoderm for head formation in the mouse. Development. 126:1999;4925-4932.
70. Shawlot W., Min Deng J., Wakamiya M., Behringer R.R. The Cerberus-related gene, Cer1, is not essential for mouse head formation. Genesis. 26:2000;253-258.
71. Shinya M., Eschbach C., Clark M., Lehrach H., Furutani-Seiki M. Zebrafish Dkk1, induced by the pre-MBT Wnt signaling, is secreted from the prechordal plate and patterns the anterior neural plate. Mech Dev. 98:2000;3-17.
72. Simeone A., Acampora D., Mallamaci A., Stornaiuolo A., D'Apice M.R., Nigro V., Boncinelli E. A vertebrate gene related to orthodenticle contains a homeodomain of the Bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 12:1993;2735-2747.
73. Stanley E.G., Biben C., Allison J., Hartley L., Wicks I.P., Campbell I.K., McKinley M., Barnett L., Koentgen F., Robb L., Harvey R.P. Targeted insertion of a LacZ reporter gene into the mouse Cer1 locus reveals complex and dynamic expression during embryogenesis. Genesis. 26:2000;259-264.
74. Summerbell D., Lewis J.H., Wolpert L. Positional information in chick limb morphogenesis. Nature. 244:1973;492-496.
75. Tam P.P., Steiner K.A. Anterior patterning by synergistic activity of the early gastrula organizer and the anterior germ layer tissues of the mouse embryo. Development. 126:1999;5171-5179.
76. Tao W., Lai E. Telencephalon-restricted expression of Bf-1, a new member of the HNF-3/fork Head gene family, in the developing rat brain. Neuron. 8:1992;957-966.
77. Thomas P., Beddington R. Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 6:1996;1487-1496.
78. Vogel A., Rodriguez C., Izpisúa Belmonte J.C. Involvement of FGF-8 in initiation, outgrowth and patterning of the vertebrate limb. Development. 2:1996;1737-1750.
79. Wallin J., Wilting J., Koseki H., Fritsch R., Christ B., Balling R. The role of Pax-1 in axial skeleton development. Development. 120:1994;1109-1121.
80. Wang S., Krinks M., Lin K., Luyten F.P., Moos M. Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell. 88:1997;757-766.
81. Wodarz A., Nusse R. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14:1998;59-88.
82. Wu W., Glinka A., Delius H., Niehrs C. Mutual antagonism between Dickkopf1 and -2 regulates Wnt/β-catenin signalling. Curr. Biol. 10:2000;1611-1614.
83. Yu K., Herr A.B., Waksman G., Ornitz D.M. Loss of fibroblast growth factor receptor 2 ligand-binding specificity in Apert syndrome. Proc. Natl. Acad. Sci. USA. 97:2000;14536-14541.
84. -/- early gastrulating mouse embryos. Proc. Natl. Acad. Sci. USA. 97:2000;14388-14393.
85. Zambrowicz B.P., Imamoto A., Fiering S., Herzenberg L.A., Kerr W.G., Soriano P. Disruption of overlapping transcripts in the ROSA β geo 26 gene trap strain leads to widespread expression of β-galactosidase in mouse embryos and hematopoietic cells. Proc. Natl. Acad. Sci. USA. 94:1997;3789-3794.
86. Zoltewicz J.S., Gerhart J.C. The Spemann organizer of Xenopus is patterned along its anteroposterior axis at the earliest gastrula stage. Dev. Biol. 192:1997;482-491.