Analysis of limb patterning in BMP-7-deficient mice

Developmental Genetics

Volumn 19, Issue 1, 1996, Pages 43-50

  Hofmann, Clementine ^a   Luo, Guangbin ^b,c   Balling, Rudi ^a   Karsenty, Gerard ^b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

BMP 7; epithelial mesenchymal interactions; homeobox and growth factor gene expression; limb development; mouse embryo

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EPITHELIUM CELL; LIMB DEFORMITY; LIMB DEVELOPMENT; MESENCHYME; MOUSE; NONHUMAN; OSSIFICATION; PHENOTYPE; POLYDACTYLY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FAMILY;

ABNORMALITIES; ANIMALS; BONE MORPHOGENETIC PROTEINS; EMBRYONIC AND FETAL DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC MARKERS; HINDLIMB; IN SITU HYBRIDIZATION; LIMB BUD; MESODERM; MICE; MICE, INBRED C3H; MICE, MUTANT STRAINS; PHENOTYPE; POLYDACTYLY;

ANIMALIA; ERINACEIDAE; VERTEBRATA;

EID: 0029763235     PISSN: 0192253X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1520-6408(1996)19:1<43::AID-DVG5>3.0.CO;2-0     Document Type: Article

References (63)

1. Bitgood MJ, McMahon AP (1995): Hedgehog and BMP genes are co-expressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol 172:126-138.
2. Chan CC, Laufer E, Tabin C, Leder P (1995): Polydactylous limbs in Strong's Luxoid mice result from ectopic polarizing activity. Development 121:1971-1978.
3. Coelho CND, Sumoy L, Rodgers BJ, Davidson DR, Hill RE, Upholt WB, Kosher RA (1991): Expression of the chicken homeobox-containing gene GHox-8 during embryonic chick limb development. Mech Dev 34:143-154.
4. Coelho CND, Sumoy L, Kosher RA, Upholt WB (1992): GHox-7: A chicken homeobox-containing gene expressed in a fashion consistent with a role in patterning events during embryonic chick limb development. Differentiation 49:85-92.
5. Cohn MJ, Izpisua-Belmonte JC, Abud H, Heath JK, Tickle C (1995): Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 80:739-746.
6. Crossley PH, Martin GR (1995): The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121:439-451.
7. Crossley PH, Minowada G, MacArthur CA, Martin GR (1996): Roles for FGF8 in the induction, initiation, and maintenance of chick limb development. Cell 84:127-136.
8. Davidson DR, Crawley A, Hill RE, Tickle C (1991): Position-dependent expression of two related homeobox genes in developing vertebrate limbs. Nature 352:429-431.
9. Davis AP, Capecchi, MR (1994): Axial homeosis and appendicular skeleton defects in mice with a targeted disruption of hoxd-11. Development 120:2187-2198.
10. Davis AP, Witte DP, Hsieh-Li HM, Potter SS, Capecchi MR (1995): Absence of radius and ulna in mice lacking hoxa-11 and hoxd-11. Nature 375:791-795.
11. Dollé P, Izpisúa-Belmonte J-C, Falkenstein H, Renucci A, Duboule D (1989): Coordinate expression of the murine Hox-5 complex homeobox-containing genes during limb pattern formation. Nature 342:767-772.
12. Dollé P, Dierich A, LeMeur M, Schimmang T, Schuhbaur B, Chambon P, Duboule D (1993): Disruption of the Hoxd-13 gene induces localized heterochrony leading to mice with neotenic limbs. Cell 75:431-441.
13. Dudley AT, Lyons KM, Robertson EJ (1995): A requirement for bone morphogenetic protein-7 during, development of the mammalian kidney and eye. Genes Dev 9:2795-2807.
14. Duprez D, Kostakopoulou K, Francis-West PH, Tickle C, Brickell P (1996): Activation of Fgf-4 and HoxD gene expression by BMP-2 expressing cells in the developing chick limb. Development. 122: 1821-1828.
15. Fallon JF, Lopez A, Ros MA, Savage MP, Olwin BB, Simandl BK (1994): FGF-2: Apical ectodermal ridge growth signal for chick limb development. Science 264:104-107.
16. Favier B, LeMeur M, Chambon P, Dollé P (1995): Axial skeleton homeosis and forelimb malformations in Hoxd-11 mutant mice. Proc Natl Acad Sci USA 92:310-314.
17. Francis PH, Richardson MK, Brickell PM, Tickle C (1994): Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development 120:209-218.
18. 3) limb buds: Their relationships in the signalling cascade involved in limb patterning. Dev Dynam 203:187-197.
19. Harland RM (1991): An improved whole-mount method for Xenopus embryos. Methods Cell Biol 36:685-695.
20. Heikinheimo M, Lawshe A, Shackleford GM, Wilson DB, MacArthur CA (1994): Fgf-8 expression in the post-gastrulation mouse embryo suggests roles in the development of the face, limbs and central nervous system. Mech Dev 48:129-138.
21. Hill RE, Jones PF, Rees AR, Sime CM, Justice MJ, Copeland MG, Jenkins NA, Graham E, Davidson DR (1989): A new family of mouse homeobox-containing genes: Molecular structure, chromosomal location and developmental expression of Hox 7.1. Genes Dev 3:26-37.
22. Hogan BLM, Blessing M, Winnier GE, Suzuki N, Jones CM (1994): Growth factors in development: The role of TGF-β related polypeptide signalling molecules in embryogenesis. Development (Suppl) 53-60.
23. Izpisúa-Belmonte J-C, Tickle C, Dolle P, Wolpert L, Duboule D (1991): Expression of the homeobox Hox-4 genes and the specification of position in chick wing development. Nature 350:585-589.
24. Izpisúa-Belmonte J-C, Brown JM, Crawley A, Duboule D, Tickle C (1992): Hox-4 gene expression in mouse/chicken heterospecific grafts of signalling regions to limb buds reveals similarities in patterning mechanisms. Development 115:553-560.
25. Johnson RL, Riddle RD, Tabin CJ (1994): Mechanisms of limb patterning. Curr Opin Genet Dev 4:535-542.
26. Jones CM, Lyons KM, Hogan BLM (1991): Involvement of Bone Morphogenetic Protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111:531-542.
27. Kingsley DM (1994): The TGF-β superfamily: New members, new receptors, and new genetic tests of function in different organisms. Genes Dev 8:133-146.
28. Laufer E, Nelson CE, Johnson RL, Morgan BA, Tabin C (1994): Sonic hedgehog and fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 79:993-1003.
29. Li H-S, Yang J-M, Jacobson RD, Pasko D, Sundin O (1994): Pax-6 is first expressed in a region of ectoderm anterior to the early neural plate: Implications for stepwise determinations of the lens. Dev Biol 162:181-194.
30. Luo G, Hofmann C, Bronckers ALJJ, Sohocki M, Bradley A, Karsenty G (1995): BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev 9:2808-2820.
31. Lyons KM, Pelton RW, Hogan BLM (1989): Patterns of expression of murine Vgr-1 and BMP-2a RNA suggest that transforming growth factor-β-like genes coordinately regulate aspects of embryonic development. Genes Dev 3:1657-1668.
32. Lyons KM, Pelton RW, Hogan BLM (1990): Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for Bone Morphogenetic Protein-2 A (BMP-2A). Development 109:833-844.
33. Lyons KM, Hogan BLM, Robertson EJ (1995): Colocalization of BMP-7 and BMP-2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech Dev 50:71-83.
34. Mahmood R, Bresnick J, Hornbruch A, Mahony C, Morton N, Colquhoun K, Martin P, Lumsden A, Dickson C, Mason I (1995): A role for FGF-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr Biol 5:797-806.
35. Masuya H, Sagai T, Wakana S, Moriwaki K, Shiroishi T (1995): A duplicated zone of polarizing activity in polydactylous mouse mutants. Genes Dev 9:1645-1653.
36. Morgan BA, Izpisúa-Belmonte J-C, Duboule D, Tabin CJ (1992): Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 358:236-239.
37. Niswander L, Martin GR (1992): FGF-4 expression during gastrulation, myogenesis, limb, and tooth development in the mouse. Development 114:755-768.
38. Niswander L, Tickle C, Vogel A, Booth I, Martin GR (1993): FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75:579-587.
39. Niswander L, Jeffrey S, Martin GR, Tickle C (1994): A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371:609-612.
40. Nohno T, Noji S, Koyama E, Ohyama K, Myokai F, Kuroiwa A, Saito T, Taniguchi S (1991): Involvement of the Chox-4 chicken homeobox genes in determination of anteroposterior axial polarity during limb development. Cell 64:1197-1205.
41. Ohuchi H, Yoshioka H, Tanaka A, Kawakami Y, Nohno T, Noji S (1994): Involvement of androgen-induced growth factor (FGF-8) gene in mouse embryogenesis and morphogenesis. Biochem Biophys Res Commun 204:882-888.
42. Ozkaynak E, Schnegelsberg PNJ, Oppermann H (1991): Murine osteogenic protein (OP-1): High level of mRNA in the kidney. Biochem Biophys Res Commun 179:116-123.
43. Parr BA, McMahon AP (1995): Dorsalizing signal WNT-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374:350-353.
44. Riddle RD, Johnson RL, Laufer E, Tabin C (1993): Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75:1401-1416.
45. Robert B, Sassoon D, Jacq B, Gehring W, Buckingham M (1989): Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. EMBO J 8:91-100.
46. Ros MA, Lyons G, Kosher RA, Upholt WB, Coelho CD, Fallon JF (1992): Apical ridge dependent and independent mesodermal domains of GHox-7 and GHox-8 expression in chick limb buds. Development 116:811-818.
47. Sampath TK, Reddi AH (1981): Dissociative extraction and reconstitution of extracellular matrix components involved in local bone differentiation. Proc Natl Acad Sci USA 78:7599-7603.
48. Sampath TK, Coughlin JE, Whetstone RM, Banach D, Corbett C, Ridge RJ, Özkaynak E, Oppermann H, Rueger DC (1990): Bovine osteogenic protein is composed of OP-1 and BMP-2A, two members of the transforming growth factor-β superfamily. J Biol Chem 265: 13198-13205.
49. Saunders JW, Gasseling MT (1968): Ectodermal-mesenchymal interactions in the origin of limb symmetry. In Fleischmajer R, Billingham RE (eds): "Epithelial-Mesenchymal Interactions." Baltimore: Williams & Wilkins, pp 78-97.
50. Song K, Wang Y, Sassoon D (1992): Expression of Hox-7.1 in myoblasts inhibits terminal differentiation and induces cell transformation. Nature 360:477-481.
51. Summerbell D, Lewis JH, Wolpert L (1973): Positional information in chick limb morphogenesis. Nature 244:492-496.
52. Tickle C, Summerbell D, Wolpert L (1975): Positional signalling and specification of digits in chick limb morphogenesis. Nature 254: 199-202.
53. Tickle C, Eichele G (1994): Vertebrate limb development. Annu Rev Cell Biol 10:121-152.
54. Todt WL, Fallon JF (1987): Posterior apical ectodermal ridge removal in the chick wing bud triggers a series of events resulting in defective anterior pattern formation. Development 101:501-515.
55. Urist MR (1965): Bone: Formation by autoinduction. Science 150: 893-899.
56. Vainio S, Karavanova I, Jovett A, Thesleff I (1993): Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during tooth development. Cell 75: 45-58.
57. Vogel A, Tickle C (1993): FGF-4 maintains polarizing activity of posterior limb bud cells in vivo and in vitro. Development 119:199-206.
58. Wall NA, Hogan BLM (1994): TGF-β-related genes in development. Curr Opin Genet Dev 4:517-522.
59. Wang Y, Sassoon D (1995): Ectoderm-mesenchyme and mesenchyme-mesenchyme interactions regulate Msx-1 expression and cellular differentiation in the murine limb bud. Dev Biol 168:374-382.
60. Wilkinson DG (1993): In situ hybridization. In Stern CD, Holland PWH (eds): "Essential Developmental Biology." Oxford: Oxford University Press, pp 257-274.
61. Winnier G, Blessing M, Labosky PA, Hogan BLM (1995): Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9:2105-2116.
62. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA (1988): Novel regulators of bone formation: Molecular clones and activities. Science 242:1528-1534.
63. Yang Y, Niswander L (1995): Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: Dorsal signals regulate anteroposterior patterning. Cell 80:939-947.