Gremlin1 induces anterior-posterior limb bifurcations in developing Xenopus limbs but does not enhance limb regeneration

Mechanisms of Development

Volumn 138, Issue , 2015, Pages 256-267

  Wang, Yi Hsuan ^a   Keenan, Samuel R ^a   Lynn, Jeremy ^a   McEwan, James C ^a   Beck, Caroline W ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Branching morphogenesis; Digit identity; Ectopic limbs; Grem1; Limb bud; Polydactyly; Regeneration; Xenopus

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GREMLIN1 PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; CKTSF1B1 PROTEIN, XENOPUS; FGF8 PROTEIN, XENOPUS; FIBROBLAST GROWTH FACTOR 8; NOGGIN PROTEIN; SHH PROTEIN, XENOPUS; SIGNAL PEPTIDE; SONIC HEDGEHOG PROTEIN; XENOPUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; FEMALE; FORELIMB; HINDLIMB; LIMB DEVELOPMENT; LIMB REGENERATION; MALE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TADPOLE; UPREGULATION; XENOPUS LAEVIS; ANIMAL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEAT SHOCK RESPONSE; LIMB; LIMB MALFORMATION; MORPHOGENESIS; PHYSIOLOGY; REGENERATION; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CARRIER PROTEINS; EXTREMITIES; FIBROBLAST GROWTH FACTOR 8; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAT-SHOCK RESPONSE; HEDGEHOG PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIMB DEFORMITIES, CONGENITAL; REGENERATION; UP-REGULATION; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84949199909     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2015.10.003     Document Type: Article

References (70)

1. Allen J.M., McGlinn E., Hill A., Warman M.L. Autopodial development is selectively impaired by misexpression of chordin-like 1 in the chick limb. Dev. Biol. 2013, 381:159-169.
2. Aoto K., Nishimura T., Eto K., Motoyama J. Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev. Biol. 2002, 251:320-332.
3. Badugu A., Kraemer C., Germann P., Menshykau D., Iber D. Digit patterning during limb development as a result of the BMP-receptor interaction. Sci. Rep. 2012, 2:991.
4. Bastida M.F., Sheth R., Ros M.A. A BMP-Shh negative-feedback loop restricts Shh expression during limb development. Development 2009, 136:3779-3789.
5. Beck C.W., Christen B., Barker D., Slack J.M. Temporal requirement for bone morphogenetic proteins in regeneration of the tail and limb of Xenopus tadpoles. Mech. Dev. 2006, 123:674-688.
6. Beck C.W., Christen B., Slack J.M. Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev. Cell 2003, 5:429-439.
7. Beck C.W., Izpisua Belmonte J.C., Christen B. Beyond early development: Xenopus as an emerging model for the study of regenerative mechanisms. Dev. Dyn. 2009, 238:1226-1248.
8. Bouldin C.M., Gritli-Linde A., Ahn S., Harfe B.D. Shh pathway activation is present and required within the vertebrate limb bud apical ectodermal ridge for normal autopod patterning. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5489-5494.
9. Brazil D.P., Church R.H., Surae S., Godson C., Martin F. BMP signalling: agony and antagony in the family. Trends Cell Biol. 2015, 25:249-264.
10. Brunet L.J., McMahon J.A., McMahon A.P., Harland R.M. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 1998, 280:1455-1457.
11. Butterfield N.C., McGlinn E., Wicking C. The molecular regulation of vertebrate limb patterning. Curr. Top. Dev. Biol. 2010, 90:319-341.
12. Capdevila J., Johnson R.L. Endogenous and ectopic expression of noggin suggests a conserved mechanism for regulation of BMP function during limb and somite patterning. Dev. Biol. 1998, 197:205-217.
13. Capdevila J., Tsukui T., Rodriquez Esteban C., Zappavigna V., Izpisua Belmonte J.C. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mol. Cell 1999, 4:839-849.
14. Chiang C., Litingtung Y., Harris M.P., Simandl B.K., Li Y., Beachy P.A., Fallon J.F. Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev. Biol. 2001, 236:421-435.
15. Chiang C., Litingtung Y., Lee E., Young K.E., Corden J.L., Westphal H., Beachy P.A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 1996, 383:407-413.
16. Christen B., Rodrigues A.M., Monasterio M.B., Roig C.F., Izpisua Belmonte J.C. Transient downregulation of Bmp signalling induces extra limbs in vertebrates. Development 2012, 139:2557-2565.
17. Christen B., Slack J.M.W. FGF-8 is associated with anteroposterior patterning and limb regeneration in Xenopus. Dev. Biol. 1997, 192:455-466.
18. Christen B., Slack J.M.W. All limbs are not the same. Nature 1998, 395:230-231.
19. Church R.H., Krishnakumar A., Urbanek A., Geschwindner S., Meneely J., Bianchi A., Basta B., Monaghan S., Elliot C., Stromstedt M., Ferguson N., Martin F., Brazil D.P. Gremlin1 preferentially binds to bone morphogenetic protein-2 (BMP-2) and BMP-4 over BMP-7. Biochem. J. 2015, 466:55-68.
20. Cuervo R., Chimal-Monroy J. Chemical activation of RARbeta induces post-embryonically bilateral limb duplication during Xenopus limb regeneration. Sci. Rep. 2013, 3:1886.
21. Eimon P.M., Harland R.M. In Xenopus embryos, BMP heterodimers are not required for mesoderm induction, but BMP activity is necessary for dorsal/ventral patterning. Dev. Biol. 1999, 216:29-40.
22. Endo T., Yokoyama H., Tamura K., Ide H. Shh expression in developing and regnerating limb buds of Xenopus leavis. Dev. Dyn. 1997, 209:227-232.
23. Fujii H., Sato T., Kaneko S., Gotoh O., Fujii-Kuriyama Y., Osawa K., Kato S., Hamada H. Metabolic inactivation of retinoic acid by a novel P450 differentially expressed in developing mouse embryos. EMBO J 1997, 16:4163-4173.
24. Geng Y., Dong Y., Yu M., Zhang L., Yan X., Sun J., Qiao L., Geng H., Nakajima M., Furuichi T., Ikegawa S., Gao X., Chen Y.G., Jiang D., Ning W. Follistatin-like 1 (Fstl1) is a bone morphogenetic protein (BMP) 4 signaling antagonist in controlling mouse lung development. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7058-7063.
25. Grow M., Neff A.W., Mescher A.L., King M.W. Global analysis of gene expression in Xenopus hindlimbs during stage-dependent complete and incomplete regeneration. Dev. Dyn. 2006, 235:2667-2685.
26. Haldin C.E., Nijjar S., Masse K., Barnett M.W., Jones E.A. Isolation and growth factor inducibility of the Xenopus laevis Lmx1b gene. Int J Dev Biol 2003, 47:253-262.
27. Han M.J., An J.Y., Kim W.S. Expression patterns of Fgf-8 during development and limb regeneration of the axolotl. Dev. Dyn. 2001, 220:40-48.
28. Harland R.M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 1991, 36:685-695.
29. Hill R.E. How to make a zone of polarizing activity: insights into limb development via the abnormality preaxial polydactyly. Develop. Growth Differ. 2007, 49:439-448.
30. Hsu D.R., Economides A.N., Wang X., Eimon P.M., Harland R.M. The Xenopus dorsalizing factor Gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol. Cell 1998, 1:673-683.
31. Jones T.E., Day R.C., Beck C.W. Attenuation of bone morphogenetic protein signaling during amphibian limb development results in the generation of stage-specific defects. J. Anat. 2013, 223:474-488.
32. Khokha M.K., Hsu D., Brunet L.J., Dionne M.S., Harland R.M. Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat. Genet. 2003, 34:303-307.
33. Kroll K.L., Amaya E. Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation. Development 1996, 122:3173-3183.
34. Li Q., Lewandowski J.P., Powell M.B., Norrie J.L., Cho S.H., Vokes S.A. A Gli silencer is required for robust repression of gremlin in the vertebrate limb bud. Development 2014, 141:1906-1914.
35. Litingtung Y., Dahn R.D., Li Y., Fallon J.F., Chiang C. Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 2002, 418:979-983.
36. Maas S.A., Fallon J.F. Single base pair change in the long-range Sonic hedgehog limb-specific enhancer is a genetic basis for preaxial polydactyly. Dev. Dyn. 2005, 232:345-348.
37. Maatouk D.M., Choi K.S., Bouldin C.M., Harfe B.D. In the limb AER Bmp2 and Bmp4 are required for dorsal-ventral patterning and interdigital cell death but not limb outgrowth. Dev. Biol. 2009, 327:516-523.
38. Maden M. Vitamin A and Pattern formation in the regenerating limb. Nature 1982, 295:672-675.
39. McEwan J., Lynch J., Beck C.W. Expression of key retinoic acid modulating genes suggests active regulation during development and regeneration of the amphibian limb. Dev. Dyn. 2011, 240:1259-1270.
40. Menshykau D., Iber D. Kidney branching morphogenesis under the control of a ligand-receptor-based Turing mechanism. Phys. Biol. 2013, 10:046003.
41. Merino R., Ganan Y., Macias D., Rodriguez-Leon J., Hurle J.M. Bone morphogenetic proteins regulate interdigital cell death in the avian embryo. Ann. N. Y. Acad. Sci. 1999, 887:120-132.
42. Metzger R.J., Krasnow M.A. Genetic control of branching morphogenesis. Science 1999, 284:1635-1639.
43. Michos O., Panman L., Vintersten K., Beier K., Zeller R., Zuniga A. Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 2004, 131:3401-3410.
44. Miura T., Shiota K., Morriss-Kay G., Maini P.K. Mixed-mode pattern in Doublefoot mutant mouse limb-Turing reaction-diffusion model on a growing domain during limb development. J. Theor. Biol. 2006, 240:562-573.
45. Newman S.M., Dumont J.N. Thiosemicarbazide-induced osteolathyrism in metamorphosing Xenopus laevis. J Exp Zool 1983, 225:411-421.
46. Nieuwkoop P.D., Faber J. A Normal Table of Xenopus laevis (Daudin) 1967, Elsevier/North Holland, Amsterdam.
47. Nishinakamura R., Sakaguchi M. BMP signaling and its modifiers in kidney development. Pediatr. Nephrol. 2014, 29:681-686.
48. Niswander L. Interplay between the molecular signals that control vertebrate limb development. Int J Dev Biol 2002, 46:877-881.
49. Norrie J.L., Lewandowski J.P., Bouldin C.M., Amarnath S., Li Q., Vokes M.S., Ehrlich L.I., Harfe B.D., Vokes S.A. Dynamics of BMP signaling in limb bud mesenchyme and polydactyly. Dev. Biol. 2014, 393:270-281.
50. Panman L., Galli A., Lagarde N., Michos O., Soete G., Zuniga A., Zeller R. Differential regulation of gene expression in the digit forming area of the mouse limb bud by SHH and gremlin 1/FGF-mediated epithelial-mesenchymal signalling. Development 2006, 133:3419-3428.
51. Pearl E.J., Barker D., Day R.C., Beck C.W. Identification of genes associated with regenerative success of Xenopus laevis hindlimbs. BMC Dev. Biol. 2008, 8:66.
52. Pignatti E., Zeller R., Zuniga A. To BMP or not to BMP during vertebrate limb bud development. Semin. Cell Dev. Biol. 2014, 32:119-127.
53. Raspopovic J., Marcon L., Russo L., Sharpe J. Modeling digits. Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients. Science 2014, 345:566-570.
54. Riddle R.D., Johnson R.L., Laufer E., Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 1993, 75:1401-1416.
55. Robert B., Lallemand Y. Anteroposterior patterning in the limb and digit specification: contribution of mouse genetics. Dev. Dyn. 2006, 235:2337-2352.
56. Saunders J.W., Gasseling M.T. Ectodermal-mesenchymal interactions in the orogin of limb symmetry. Epithelial-Mesenchymal Interactions 1968, 78-97. Williams and Wilkins, Baltimore. R. Fleischmajer (Ed.).
57. Scadding S.R., Maden M. The effects of local application of retinoic acid in limb development and regeneration in tadpoles of Xenopus laevis. J. Embryol. Exp. Morphol. 1986, 91:55-63.
58. Scherz P.J., Harfe B.D., McMahon A.P., Tabin C.J. The limb bud Shh-Fgf feedback loop is terminated by expansion of former ZPA cells. Science 2004, 305:396-399.
59. Summerbell D. A quantitative analysis of the effect of excision of the AER from the chick limb-bud. J. Embryol. Exp. Morpholog. 1974, 32:651-660.
60. Tanaka S., Iber D. Inter-dependent tissue growth and Turing patterning in a model for long bone development. Phys. Biol. 2013, 10:056009.
61. Tarin D., Sturdee A.P. Early limb development of Xenopus laevis. J. Embryol Exp Morphol. 1971, 26:169-179.
62. Tickle C. The number of polarizing region cells required to specify additional digits in the developing chick wing. Nature 1981, 289:295-298.
63. Towers M., Wolpert L., Tickle C. Gradients of signalling in the developing limb. Curr. Opin. Cell Biol. 2012, 24:181-187.
64. Tschumi P.A. The growth of the hindlimb bud of Xenopus laevis and its dependence upon the epidermis. J. Anat. 1957, 91:149-173.
65. Verheyden J.M., Sun X. An Fgf/Gremlin inhibitory feedback loop triggers termination of limb bud outgrowth. Nature 2008, 454:638-641.
66. Wang Y.H., Beck C.W. Distal expression of sprouty (spry) genes during Xenopus laevis limb development and regeneration. Gene Expr. Patterns 2014, 15:61-66.
67. Wordinger R.J., Zode G., Clark A.F. Focus on molecules: gremlin. Exp. Eye Res. 2008, 87:78-79.
68. Zeller R., Lopez-Rios J., Zuniga A. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat. Rev. Genet. 2009, 10:845-858.
69. Zuniga A., Haramis A.P., McMahon A.P., Zeller R. Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature 1999, 401:598-602.
70. Zuniga A., Michos O., Spitz F., Haramis A.P., Panman L., Galli A., Vintersten K., Klasen C., Mansfield W., Kuc S., Duboule D., Dono R., Zeller R. Mouse limb deformity mutations disrupt a global control region within the large regulatory landscape required for Gremlin expression. Genes Dev. 2004, 18:1553-1564.