Essential pro-Bmp roles of crossveinless 2 in mouse organogenesis

Development

Volumn 133, Issue 22, 2006, Pages 4463-4473

  Ikeya, Makoto ^a   Kawada, Masako ^a   Kiyonari, Hiroshi ^a   Sasai, Noriaki ^a   Nakao, Kazuki ^a   Furuta, Yasuhide ^b   Sasai, Yoshiki ^a  

^a RIKEN   (Japan)

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

Author keywords

Crim2; Crossveinless 2 (Bmper); Gene targeting; Mouse; Organogenesis

Indexed keywords

BINDING PROTEIN; BONE MORPHOGENETIC PROTEIN 4; CROSSVEINLESS 2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEFECT; BONE DEVELOPMENT; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EYE DEVELOPMENT; FIBROBLAST CULTURE; GASTRULATION; GENE DELETION; GENE EXPRESSION; KIDNEY DEVELOPMENT; KIDNEY HYPOPLASIA; MOUSE; MOUSE MUTANT; NEPHRON; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPINE;

ANIMALS; CARRIER PROTEINS; CARTILAGE; DNA PRIMERS; EYE; IMMUNOHISTOCHEMISTRY; KIDNEY; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; ORGANOGENESIS; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 33845866050     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02647     Document Type: Article

References (74)

1. Aruga, J., Mizugishi, K., Koseki, H., Imai, K., Balling, R., Noda, T. and Mikoshiba, K. (1999). Zic1 regulates the patterning of vertebral arches in cooperation with Gli3. Mech. Dev 89, 141-150.
2. Ashe, H. L. and Levine, M. (1999). Local inhibition and long-range enhancement of Dpp signal transduction by Sog. Nature 398, 427-431.
3. Bachiller, D., Klingensmith, J., Shneyder, N., Tran, U., Anderson, R., Rossant, J. and De Robertis, E. M. (2003). The role of chordin/Bmp signals in mammalian pharyngeal development and DiGeorge syndrome. Development 130, 3567-3578.
4. Binnerts, M. E., Wen, X., Cante-Barrett, K., Bright, J., Chen, H. T., Asundi, V., Sattari, P., Tang, T., Boyle, B., Funk, W. et al. (2004). Human Crossveinless-2 is a novel inhibitor of bone morphogenetic proteins. Biochem. Biophys. Res. Commun. 315, 272-280.
5. Canalis, E., Economides, A. N. and Gazzerro, E. (2003). Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr. Rev. 24, 218-235.
6. Cheah, K. S., Lau, E. T, Au, P. K. and Tam, P. P. (1991). Expression of the mouse alpha 1 (II) collagen gene is not restricted to cartilage during development. Development 111, 945-953.
7. Coffinier, C., Ketpura, N., Tran, U., Geissert, D. and De Robertis, E. M. (2002). Mouse Crossveinless-2 is the vertebrate homolog of a Drosophila extracellular regulator of BMP signaling. Mech. Dev 119, S179-S1084.
8. Coles, E., Christiansen, J., Economou, A., Bronner-Fraser, M. and Wilkinson, D. G. (2004). A vertebrate crossveinless 2 homologue modulates BMP activity and neural crest cell migration. Development 131, 5309-5317.
9. Conley, C. A., Silburn, R., Singer, M. A., Ralston, A., Rohwer-Nutter, D., Olson, D. J., Gelbart, W. and Blair, S. S. (2000). Crossveinless 2 contains cysteine-rich domains and is required for high levels of BMP-like activity during the formation of the cross veins in Drosophila. Development 127, 3947-3959.
10. Dale, L., Howes, G., Price, B. M. J. and Smith, J. C. (1992). Bone morphogenetic protein 4, a ventralizing factor in early Xenopus development. Development 115, 573-585.
11. Decotto, E. and Ferguson, E. L. (2001). A positive role for Short gastrulation in modulating BMP signaling during dorsoventral patterning in the Drosophila embryo. Development 128, 3831-3841.
12. Delot, E. C., Bahamonde, M. E., Zhao, M. and Lyons, K. M. (2003). BMP signaling is required for septation of the outflow tract of the mammalian heart. Development 130, 209-220.
13. De Robertis, E. M. and Sasai, Y. (1996). A common plan for dorsoventral patterning in Bilateria. Nature 380, 37-40.
14. Dudley, A. T., Lyons, K. M. and Robertson, E. J. (1995). A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 9, 2795-2807.
15. Fainsod, A., Steinbeisser, H. and De Robertis, E. M. (1994). On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO J. 13, 5015-5025.
16. Ferguson, E. L. and Anderson, K. (1992a). decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71, 451-461.
17. Ferguson, E. L. and Anderson, K. (1992b). Localized enhancement and repression of the activity of the TGF-beta family member, decapentaplegic, is necessary for dorso-ventral pattern formation in the Drosophila embryo. Development 114, 583-597.
18. Fisher, S., Amacher, S. L. and Halpern, M. E. (1997). Loss of cerebrum function ventralizes the zebrafish embryo, Development 124, 1301-1311.
19. François, V., Solloway, M., O'Neill, J. W., Emery, J. and Bier, E. (1994). Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the shortgastrulation gene. Genes Dev. 8, 2602-2616.
20. Garcia-Bellido, A. and de Celis, J. F. (1992). Developmental genetics of the venation pattern of Drosophila. Annu. Rev. Genet. 26, 277-304.
21. Glinka, A., Wu, W., Onichtchouk, D., Blumenstock, C. and Niehrs, C. (1997). Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus. Nature 389, 517-519.
22. Glumoff, V., Savontaus, M., Vehanen, J. and Vuorio, E. (1994). Analysis of aggrecan and tenascin gene expression in mouse skeletal tissues by northern and in situ hybridization using species specific cDNA probes. Biochim. Biophys. Acta 1219, 613-622.
23. Godin, R. E., Takaesu, N. T., Robertson, E. J. and Dudley, A. T. (1998). Regulation of BMP7 expression during kidney development. Development 125, 3473-3482.
24. Godin, R. E., Robertson, E. J. and Dudley, A. T. (1999). Role of BMP family members during kidney development. Int. J. Dev. Biol. 43, 405-411.
25. Goldman, D. C., Hackenmiller, R., Nakayama, T., Sopory, S., Wong, C., Kulessa, H. and Christian, J. L. (2006). Mutation of an upstream cleavage site in the BMP4 prodomain leads to tissue-specific loss of activity. Development 133, 1933-1942.
26. Grieshammer, U., Cebrian, C., Ilagan, R., Meyers, E., Herzlinger, D. and Martin, G. R. (2005). FGF8 is required for cell survival at distinct stages of nephrogenesis and for regulation of gene expression in nascent nephrons. Development 132, 3847-3857.
27. Gurdon, J. B. and Bourillot, P. Y. (2001). Morphogen gradient interpretation. Nature 413, 797-803.
28. Hammerschmidt, M. and Mullins, M. C. (2002). Dorsoventral patterning in the zebrafish: bone morphogenetic proteins and beyond. In Pattern Formation in Zebrafish (ed. L. Solnica-Krezel), pp. 72-95. Berlin, Heidelberg: Springer-Verlag
29. Hemmati-Brivanlou, A., Kelly, O. G. and Melton, D. A. (1994). Follistatin, an antagonist of activin is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77, 283-295.
30. Hogan, B. L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 10, 1580-1594.
31. Hogan, B., Beddington, R., Costantini, F. and Lacy, E. (1994). Manipulating the Mouse Embryo (2nd edn). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
32. Hsu, D. R., Economides, A. N., Wang, X., Eimon, P. M. and Harland, R. M. (1998). The Xenopus dorsalizing factor Gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol. Cell 1, 673-683.
33. Ikeya, M. and Takada, S. (1998). Wnt signaling from the dorsal neural tube is required for the formation of the medial dermomyotome. Development 125, 4969-4976.
34. Ikeya, M., Kawada, M., Nakazawa, Y., Sakuragi, M., Sasai, N., Ueno, M., Kiyonari, H., Nakao, K. and Sasai, Y. (2005). Gene disruption/knock-in analysis of mONT3: vector construction by employing both in vivo and in vitro recombinations. Int. J. Dev. Biol. 49, 807-823.
35. Jena, N., Martin-Seisdedos, C., McCue, P. and Croce, C. M. (1997). BMP7 null mutation in mice: developmental defects in skeleton, kidney, and eye. Exp. Cell Res. 230, 28-37.
36. Jones, C. M., Lyons, K. M., Lapan, R M., Wright, C. V. E. and Hogan, B. L. M. (1992). DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction. Development 115, 639-647.
37. Kamimura, M., Matsumoto, K., Koshiba-Takeuchi, K. and Ogura, T. (2004). Vertebrate crossveinless 2 is secreted and acts as an extracellular modulator of the BMP signaling cascade, Dev Dyn. 230, 434-445.
38. Lamb, T. M., Knecht, A. K., Smith, W. C., Stachel, S. E., Economides, A. N., Stahl, N., Yancopolous, G. D. and Harland, R. M. (1993). Neural induction by the secreted polypeptide noggin. Science 262, 713-718.
39. Larrain, J., Bachiller, D., Lu, B., Agius, E., Piccolo, S. and De Robertis, E. M. (2000). BMP-binding modules in chordin: a model for signalling regulation in the extracellular space. Development 127, 821-830.
40. Lawson, K. A., Dunn, N. R., Roelen, B. A., Zeinstra, L. M., Davis, A. M., Wright, C. V., Korving, J. P. and Hogan, B. L. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13, 424-436.
41. Lee, K. J. and Jessell, T. M. (1999). The specification of dorsal cell fates in the vertebrate central nervous system. Annu. Rev. Neurosci. 22, 261-294.
42. Lengner, C. J., Lepper, C., van Wijnen, A. J., Stein, J. L., Stein, G. S. and Lian, J. B. (2004). Primary mouse embryonic fibroblasts: a model of mesenchymal cartilage formation. J. Cell Physiol. 200, 327-333.
43. Lin, J., Patel, S. R., Cheng, X., Cho, E. A., Levitan, I., Ullenbruch, M., Phan, S. H., Park, J. M. and Dressler, G. R. (2005). Kielin/ chordin-like protein, a novel enhancer of BMP signaling, attenuates renal fibrotic disease. Nat. Med. 11, 387-393.
44. Luo, G., Hofmann, C., Bronckers, A. L., Sohocki, M., Bradley, A. and 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.
45. Massague, J. and Chen, Y. G. (2000). Controlling TGF-beta signaling. Genes Dev. 14, 627-644.
46. Matsui, M., Mizuseki, K., Nakatani, J., Nakanishi, S. and Sasai, Y. (2000). Xenopus kielin: A dorsalizing factor containing multiple chordin-type repeats secreted from the embryonic midline. Proc. Natl. Acad. Sci. USA 97, 5291-5296.
47. Miyazaki, Y., Oshima, K., Fogo, A., Hogan, B. L. and Ichikawa, I. (2000). Bone morphogenetic protein 4 regulates the budding site and elongation of the mouse ureter. J. Clin. Invest. 105, 863-873.
48. Mizuseki, K., Sakamoto, T., Watanabe, K., Muguruma, K., Ikeya, M., Nishiyama, A., Arakawa, A., Suemori, H., Nakatsuji, N., Kawasaki, H. et al. (2003). Generation of neural crest-derived peripheral neurons and floor plate cells from mouse and primate embryonic stem cells. Proc. Natl. Acad. Sci. USA 100, 5828-5833.
49. Moser, M., Binder, O., Wu, Y., Aitsebaomo, J., Ren, R., Bode, C., Bautch, V. L., Conlon, F. L. and Patterson, C. (2003). BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol. Cell. Biol. 23, 5664-5679.
50. Murtaugh, L. C., Chyung, J. H. and Lassar, A. B. (1999). Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev 13, 225-237.
51. Nosaka, T, Morita, S., Kitamura, H., Nakajima, H., Shibata, F., Morikawa, Y., Kataoka, Y., Ebihara, Y., Kawashima, T., Itoh, T. et al. (2003). Mammalian twisted gastrulation is essential for skeleto-lymphogenesis. Mol. Cell. Biol. 23, 2969-2980.
52. O'Connor, M. B., Umulis, D., Othmer, H. G. and Blair, S. S. (2006). Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133, 183-193.
53. Parr, B. A. and McMahon, A. P. (1995). Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374, 350-353.
54. Petryk, A., Anderson, R. M., Jarcho, M. P., Leaf, I., Carlson, C. S., Klingensmith, J., Shawlot, W. and O'Connor, M. B. (2004). The mammalian twisted gastrulation gene functions in foregut and craniofacial development. Dev. Biol. 267, 374-386.
55. Ralston, A. and Blair, S. S. (2005). Long-range Dpp signaling is regulated to restrict BMP signaling to a crossvein competent zone. Dev. Biol. 280, 187-200.
56. Rentzsch, F., Zhang, J., Kramer, C., Sebald, W. and Hammerschmidt M. (2006). Crossveinless 2 is an essential positive feedback regulator of Bmp signaling during zebrafish gastrulation. Development 133, 801-811.
57. Sasai, Y., Lu, B., Steinbeisser, H., Geissert, D., Gont, L. K. and De Robertis, E. M. (1994). Xenopus chordin: a novel clorsalizing factor activated by organizer-specific homeoboxes genes. Cell 79, 779-790.
58. Sasai, Y., Lu, B., Steinbeisser, H. and De Robertis, E. M. (1995). Regulation of neural induction by the chd and BMP-4 antagonistic patterning signals in Xenopus. Nature 376, 333-336.
59. Schulte-Merker, S., Lee, K. J., McMahon, A. P. and Hammerschmidt, M. (1997). The zebrafish organizer requires chordino. Nature 387, 862-863.
60. Simic, R and Vukicevic, S. (2005). Bone morphogenetic proteins in development and homeostasis of kidney. Cytokine Growth Factor Rev 16, 299-308,
61. Smith, W. C. and Harland, R. M. (1992). Expression cloning of noggin, a new clorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829-840.
62. Su, H. L., Muguruma, K., Matsuo-Takasaki, M., Kengaku, M., Watanabe, K. and Sasai, Y. (2006). Generation of cerebellar neuron precursors from embryonic stem cells. Dev. Biol. 290, 287-296.
63. Suzuki, N., Labosky, P. A., Furuta, Y., Hargett, L., Dunn, R., Fogo, A. B., Takahara, K., Peters, D. M., Greenspan, D. S. and Hogan, B. L. (1996). Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid. Development 122, 3587-3595.
64. Wagner, D. S. and Mullins, M. C. (2002). Modulation of BMP activity in dorsalventral pattern formation by the chordin and ogon antagonists. Dev. Biol. 245, 109-123.
65. Wan, M. and Cao, X. (2005). BMP signaling in skeletal development. Biochem. Biophys. Res. Commun. 328, 651-657.
66. Weaver, M., Yingling, J. M., Dunn, N. R., Bellusci, S. and Hogan, B. L. (1999). Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development. Development 126, 4005-4015.
67. Weaver, M., Batts, L. and Hogan, B. L. (2003). Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev Biol. 258, 169-184.
68. Wharton, K. A., Ray, R. P. and Gelbart, W. M. (1993). The activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117, 807-822.
69. Yagi, T., Tokunaga, T., Furuta, Y., Nada, S., Yoshida, M., Tsukada, T., Saga, Y., Takeda, N., Ikawa, Y. and Aizawa, S. (1993a). A novel ES cell line, TT2, with high germline-differentiating potency Anal. Biochem. 214, 70-76.
70. Yagi, T., Nada, S., Watanabe, N., Tamemoto, H., Kohmura, N., Ikawa, Y. and Aizawa, S. (1993b). A novel negative selection for homologous recombinants using diphtheria toxin A fragment gene. Anal. Biochem. 214, 77-86.
71. Yi, S. E., Daluiski, A., Pederson, R., Rosen, V. and Lyons, K. M. (2000). The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 127, 621-630.
72. Zakin, L. and De Robertis, E. M. (2004). Inactivation of mouse Twisted gastrulation reveals its role in promoting Bmp4 activity during forebrain development. Development 131, 413-424.
73. Zakin, L., Reversade, B., Kuroda, H., Lyons, K. M. and De Robertis, E. M. (2005). Sirenomelia in Bmp7 and Tsg compound mutant mice: requirement for Bmp signaling in the development of ventral posterior mesoderm. Development 132, 2489-2499.
74. Zusman, S. B., Sweeton, D. and Wieschaus, E. F. (1988). short-gastrulation, a mutation causing delays in stage-specific cell shape changes during gastrulation in Drosophila melanogaster. Dev. Biol. 129, 417-442.