Targeted misexpression of constitutively active BMP receptor-IB causes bifurcation, duplication, and posterior transformation of digit in mouse limb

Developmental Biology

Volumn 220, Issue 2, 2000, Pages 154-167

  Zhang, Zunyi ^a   Yu, Xueyan ^b   Zhang, Yanding ^b   Geronimo, Benedicto ^a   Løvlie, Arne ^a   Fromm, Sigurd H ^a   Chen, Yiping ^b  

^a UNIVERSITY OF OSLO   (Norway)

^b Tulane University   (United States)

Author keywords

Apoptosis; BMP; BMP receptor; Limb patterning; Transgenic mice

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR; RECEPTOR SUBTYPE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; EMBRYO; FINGER; GENE OVEREXPRESSION; LIMB DEVELOPMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; RIB; STERNUM; TRANSGENIC MOUSE;

ANIMALIA; ERINACEIDAE; MUS MUSCULUS; VERTEBRATA;

EID: 0034656111     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.2000.9637     Document Type: Article

References (81)

1. Becker D., Jiang Z., Knodler P., Dienard A. S., Eid R., Kidd K. K., Shashikant C. S., Ruddle F. H., Schughart K. Conserved regulatory element involved in the early onset of Hoxb6 gene expression. Dev. Dyn. 205:1996;73-81.
2. Brunet L. J., McMahon J. A., McMahon A. P., Harland R. M. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science. 280:1998;1455-1457.
3. Buckland R. A., Collinon J. M., Graham E., Hill R. E. Antagonistic effects of FGF4 and BMP induction of apoptosis and chondrogenesis in chick limb bud. Mech. Dev. 71:1998;143-150.
4. 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. 197:1998;205-217.
5. 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.
6. Chang D. T., Lopez A., von Kessler D. P., Chiang C., Simandl B. K., Zhao R., Seldin M. F., Fallon J. F., Beachy P. A. Products, genetic linkage and limb patterning activity of a murine hedgehog gene. Development. 120:1994;3339-3353.
7. Charité J., de Graaff W., Shen S., Deschamps J. Ectopic expression of Hoxb-8 cause duplication of the ZPA in the forelimb and homeotic transformation of axial structures. Cell. 78:1994;589-601.
8. Chen J. M. Studies on the morphogenesis of the mouse sternum. I. Normal embryonic development. J. Anat. London. 86:1952a;373-386.
9. Chen J. M. Studies on the morphogenesis of the mouse sternum. II. Experiments on the origin of the sternum and its capacity for self-differentiation in vitro. J. Anat. London. 86:1952b;387-401.
10. Chen Y. P., Zhao X. Shaping limbs by apoptosis. J. Exp. Zool. 282:1998;691-702.
11. 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. 121:1995;439-451.
12. Crossley P. H., Minowada G., MacArthur C. A., Martin G. R. Roles for FGF8 in the induction, initiation and maintenance of chick limb development. Cell. 84:1996;127-136.
13. Dewulf N., Verschueren K., Lonnoy O., Morén A., Grimsby S., Spiegle K. V., Miyazono K., Huylebroeck D., ten Dijik P. Distinct spatial and temporal expression patterns of two type I receptors for bone morphogenetic proteins during mouse embryogenesis. Endocrinology. 136:1995;2652-2663.
14. Dudley A. T., Lyons K. M., Robertson E. J. A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 9:1995;2795-2807.
15. Duprez D. M., Bell E. J., Richardson M., Archer C. W., Wolpert L., Brickell P. M., Francis-West P. H. Overexpression of BMP-2 and BMP-4 alters the size and shape of developing skeletal elements in the chick limb. Mech. Dev. 57:1996a;145-157.
16. Duprez D. M., Kostakopoulou K., Francis-West P. H., Tickle C. Activation of Fgf-4 and HoxD gene expression by Bmp-2 expressing cells in the developing limb. Development. 122:1996b;1821-1828.
17. Eid R., Koseki H., Schughart K. Analysis of LacZ reporter genes in transgenic embryos suggests the presence of several cis-acting regulatory elements in the murine Hoxb-6 gene. Dev. Dyn. 196:1993;205-216.
18. Fallon J. F., Lopez A., Ros M. A., Savage M. P., Olwin B. B., Simandl B. K. FGF-2: Apical ectodermal ridge growth signal for chick limb development. Science. 264:1994;104-107.
19. Francis P. H., Richardson M. K., Brickell P. M., Tickle C. Bone morphogenetic proteins and a signaling pathway that controls patterning in the developing chick limb. Development. 120:1994;209-218.
20. Francis-West P. H., Robertson K. E., Ede D. E., Rodriguez C., Izpisúa-Belmonte J. C., Houston B., Burt D. W., Gribbin C., Brickell P. M., Tickle C. Expression of genes encoding bone morphogenetic proteins and sonic hedgehog in Talpid (ta3) limb buds: Their relationships in the signaling cascade involved in limb patterning. Dev. Dyn. 203:1995;187-197.
21. Goff D. J., Tabin C. J. Analysis of Hoxd-13 and Hoxd-11 misexpression in chick limb buds reveals that Hox genes affect both bone condensation and growth. Development. 124:1997;627-636.
22. Graham A., Francis-West P., Brickell P., Lumsden A. The signaling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest. Nature. 372:1994;684-686.
23. Gañan Y., Macias D., Duterque-Coquillaud M., Ros M. A., Hurle J. M. Role of TGF-βs and BMPs as signals controlling the position of the digits and the areas of cell death in the developing chick limb autopod. Development. 122:1996;2349-2357.
24. Hinchliffe J. R., Johnson D. R. The Development of the Vertebrate Limb. 1980;Oxford Univ. Press, Oxford.
25. Hogan B. L. M. Bone morphogenetic proteins: Multifunctional regulators of vertebrate development. Genes Dev. 10:1996;1580-1594.
26. Hogan B., Beddington R., Costantini F., Lacy E. Manipulating the Mouse Embryo: A Laboratory Manual. 1994;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
27. Hoodless P. A., Haerry T., Abodollah S., Stapleton M., O'Connor M. B., Attisano L., Wrana J. L. MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell. 85:1996;489-500.
28. Huang R., Zhi Q., Neubuser A., Muller T. S., Brand-Saberi B., Christ B., Wilting J. Function of somite and somitocoel cells in the formation of the vertebral motion segment in avian embryo. Acta Anat. (Basel). 155:1996;231-241.
29. Ingham P. W., Fietz M. J. Quantitative effects of hedgehog and decapentaplegic activity on the patterning of the Drosophila wing. Curr. Biol. 5:1995;432-440.
30. Jervall J., Åberg T., Kettunen P., Keränen S., Thesleff I. The life history of an embryonic signaling center: BMP-4 induces p21 and is associated with apoptosis in the mouse tooth enamel knot. Development. 125:1998;161-169.
31. Jones C. M., Lyons K., Hogan B. L. M. Involvement of bone morphogenetic protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development. 111:1991;531-542.
32. Kawakami Y., Ishikawa T., Shimabara M., Tanda N., Enomoto-Iwamoto M., Iwamoto M., Kuwana T., Ueki A., Noji S., Nohno T. BMP signaling during bone pattern determination in the developing limb. Development. 122:1996;3557-3566.
33. Knezevic V., Santo R. D., Schughart K., Huffstadt U., Chiang C., Mahon K. A., Mackem S. Hoxd-12 differentially affects preaxial and postaxial chondrogenic branches in the limb and regulates Sonic hedgehog in a positive feedback loop. Development. 124:1997;4523-4536.
34. Koenig B. B., Cook J. S., Wolsing D. H., Ting J., Tiesman J. P., Correa P. E., Olson C. A., Pecquet A. L., Ventura F., Grant R. A., Chen G. X., Wrana J. L., Massagué J., Rosenbaum J. S. Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol. Cell. Biol. 14:1994;5961-5974.
35. Kretzschmar M., Liu F., Hata A., Doody J., Massagué J. The TGFβ family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11:1997;984-995.
36. Laufer E., Nelson C. E., Johnson R. L., Morgan B. A., Tabin C. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell. 79:1994;993-1003.
37. Liu F., Ventura F., Doody J., Massagué J. Human type II receptor for bone morphogenetic proteins (BMPs): Extension of the two-kinase receptor model for the BMPs. Mol. Cell. Biol. 15:1995;3479-3486.
38. Luo G., Hofmann C., Bronckers A. L. J. J., 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.
39. Lyons K., Hogan B. L. M., Robertson E. J. Colocalization of BMP7 and BMP2 suggests that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev. 50:1995;71-83.
40. Lyons K., Pelton R. W., Hogan B. L. M. Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for bone morphogenetic protein-2A (BMP-2A). Development. 109:1990;833-844.
41. Macias D., Gañan Y., Sampath T. K., Piedra M. E., Ros M. A., Hurle J. M. Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development. Development. 124:1997;1109-1117.
42. Marazzi G., Wang Y., Sassoon D. Msx2 is a transcriptional regulator in the BMP4-mediated programmed cell death pathway. Dev. Biol. 186:1997;127-138.
43. Massagué J. TGFβ signaling: Receptors, transducers, and Mad protein. Cell. 85:1996;947-950.
44. Merino R., Rodriguez-Leon J., Macias D., Gañan Y., Economides A. N., Hurle J. M. The BMP antagonist Gremlin regulates ourgrowth, chondrogenesis and programmed cell death in the developing limb. Development. 126:1999;5515-5522.
45. Mishina Y., Susuki A., Ueno N., Behringer R. R. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 9:1995;3027-3037.
46. Morgan B. A., Izpisúa-Belmonte J.-C., Duboule D., Tabin C. J. Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformation. Nature. 358:1992;236-239.
47. Niswander L., Jeffrey S., Martin G. R., Tickle C. A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature. 371:1994;609-612.
48. Niswander L., Martin G. R. FGF-4 and BMP-2 have opposite effects on limb growth. Nature. 361:1993;68-71.
49. Niswander L., Tickle C., Vogel A., Booth I., Martin G. R. FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell. 75:1993;579-587.
50. Nohno T., Ishikawa T., Saito T., Hosokawa K., Noji S., Wolsing D. H., Rosenbaum J. S. Identification of a human type II receptor for bone morphogenetic protein-4 that forms differential heteromeric complexes with bone morphogenetic protein type I receptors. J. Biol. Chem. 270:1995;22,522-22,526.
51. Ohuchi H., Nakagawa T., Yamamoto A., Araga A., Ohata T., Ishimaru Y., Yoshioka H., Kuwana T., Nohno T., Yamasaki M., Itoh N., Noji S. The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development. 124:1997;2235-2244.
52. Parr B. A., McMahon A. P. Dorsaling signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature. 374:1995;350-353.
53. Pearse R. V. II, Tabin C. J. The molecular ZPA. J. Exp. Zool. 282:1998;677-690.
54. Qu S., Niswender K. D., Ji Q., van der Meer R., Keeney D., Magnuson M. A., Wisdom R. Polydactyly and ectopic ZPA formation in Alx-4 mutant mice. Development. 124:1997;1089-1098.
55. Qu S., Tucker S. C., Ehrlich J. S., Levorse J. M., Flaherty L. A., Wisdom R., Vogt T. Mutations in mouse Aristaless-like4 cause Strong's luxoid polydactyly. Development. 125:1998;2711-2721.
56. Riddle R. D., Ensini M., Nelson C., Tsuchida T., Jessell T. M., Tabin C. Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell. 83:1995;631-640.
57. Riddle R. D., Johnson R. L., Laufer E., Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 75:1993;1401-1416.
58. Rosenzweig B. L., Imamura T., Okadome T., Cox G. N., Yamashita H., ten Dijke P., Heldin C. H., Miyazono K. Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc. Natl. Acad. Sci. USA. 92:1995;7632-7636.
59. Saunders J. W. Jr., Gasseling M. T. Ectoderm-mesenchymal interaction in the origins of wing symmetry. Fleischmajer R., Billingham R. E. Epithelial-Mesenchymal Interactions. 1968;78-97 Williams & Wilkins, Baltimore.
60. Schughart K., Bieberich C. J., Eid R., Ruddle F. H. A regulatory region from the mouse Hox-2.2 promoter directs gene expression into developing limbs. Development. 112:1991;807-811.
61. Sumitomo S., Saito T., Nohno T. A new receptor protein kinase from chick embryo related to type II receptor for TGF-beta. DNA Seq. 3:1993;297-302.
62. Takahashi M., Tamura K., Büscher D., Masuya H., Yonei-Tamura S., Matsumoto K., Naitoh-Matsuo M., Takeuchi J., Ogura K., Shiroishi T., Ogura T., Izpisúa-Belmonte J. C. The role of Alx-4 in the establishment of anteroposterior polarity during vertebrate limb development. Development. 125:1998;4417-4425.
63. ten Dijke P., Yamashita H., Ichijo H., Franzén P., Laiho M., Miyazono K., Heldin C.-H. Characterization of type I receptors for transforming growth factor-β and activin. Science. 264:1994a;101-104.
64. ten Dijke P., Yamashita H., Sampath T. K., Reddi A. H., Estevez M., Riddle D. L., Ichijo H., Heldin C. H., Miyazono K. Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J. Biol. Chem. 269:1994b;16,985-16,988.
65. Tickle C. Genetics and limb development. Dev. Genet. 19:1996;1-8.
66. Urist M. R., Mikulski A., Lietze A. Solubilized and insolubilized bone morphogenetic protein. Proc. Natl. Acad. Sci. USA. 76:1979;1828-1832.
67. Vogel A., Rodriguez C., Izpisua-Belmonte J. C. Involvement of FGF-8 in initation, outgrowth and patterning of the vertebrate limb. Development. 122:1996;1737-1750.
68. Vogel A., Rodriguez C., Warnken W., Izpisúa-Belmonte J. C. Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature. 378:1995;716-720.
69. Wieser R., Wrana J. L., Massagué J. GS domain mutations that constitutively activate TβR-1, the downstream signaling component in the TGF-β receptor complex. EMBO J. 14:1995;2199-2208.
70. Winnier G., Blessing M., Labosky P. A., Hogan B. L. M. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9:1995;2105-2116.
71. Wozney J. M., Capparella J., Rosen V. The bone morphogenetic proteins in cartilage and bone development. Bernfield M. Molecular Basis of Morphogenesis. 1993;221-230 Wiley-Liss, New York.
72. Wozney J. M., Rosen V., Celeste A. J., Mitsock L. M., Whiters M. J., Kris R. W., Hewick R. M., Wang E. A. Novel regulator of bone formation: Molecular clones and activities. Science. 242:1988;1528-1534.
73. Yang Y., Drossopoulou G., Chuang P.-T., Duprez D., Marti E., Bumcrot D., Vargesson N., Clarke J., Niswander L., McMahon A., Tickle C. Relationship between distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development. 124:1997;4393-4404.
74. Yang Y., Niswander L. Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: dorsal signals regulate anterior-posterior patterning. Cell. 80:1995;939-947.
75. Yokouchi Y., Sakiyama J., Kameda T., Iba H., Suzuki A., Ueno N., Kuroiwa A. BMP-2/-4 mediate programmed cell death in chicken limb buds. Development. 122:1996;3725-3734.
76. Zhang H., Bradley A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development. 122:1996;2977-2985.
77. Zhang Y. D., Zhang Z. Y., Zhao X., Yu X., Hu Y., Geronimo B., Fromm S. H., Chen Y. P. A new function of BMP4: Dual role for BMP4 in regulation of Sonic hedgehog expression in the mouse tooth germ. Development. 2000.
78. Zhang Z. Y., Balmer J. E., Løvlie A., Fromm S. H., Blomhoff R. Specific teratogenic effects of different retinoic acid isoforms and analogs in the developing anterior central nervous system of zebrafish. Dev. Dyn. 206:1996;70-86.
79. Zou H., Niswander L. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science. 272:1996;738-741.
80. Zou H., Wieser R., Massagué J., Niswander L. Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 11:1997;2191-2203.
81. Zúñiga A., Haramis A.-P. G., McMahon A. P., Zeller R. Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature. 401:1999;598-601.