Two novel type II receptors mediate BMP signalling and are required to establish left-right asymmetry in zebrafish

Developmental Biology

Volumn 315, Issue 1, 2008, Pages 55-71

  Monteiro, Rui ^a   van Dinther, Maarten ^b   Bakkers, Jeroen ^a,c   Wilkinson, Robert ^d   Patient, Roger ^d   ten Dijke, Peter ^b   Mummery, Christine ^a,c  

^a HUBRECHT INSTITUTE   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

bmpr2a; bmpr2b; Cardiac laterality; Left right asymmetry; Visceral laterality; Zebrafish

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR; BONE MORPHOGENETIC PROTEIN RECEPTOR 2A; BONE MORPHOGENETIC PROTEIN RECEPTOR 2B; PROTEIN LEFTY1; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR PITX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; MESODERM; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ZEBRA FISH;

DANIO RERIO; VERTEBRATA;

EID: 39249085586     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.11.038     Document Type: Article

References (65)

1. Albertson R.C., Payne-Ferreira T.L., Postlethwait J., and Yelick P.C. Zebrafish acvr2a and acvr2b exhibit distinct roles in craniofacial development. Dev. Dyn. 233 (2005) 1405-1418
2. Amack J.D., and Yost H.J. The T box transcription factor no tail in ciliated cells controls zebrafish left-right asymmetry. Curr. Biol. 14 (2004) 685-690
3. Beppu H., Minowa O., Miyazono K., and Kawabata M. cDNA cloning and genomic organization of the mouse BMP type II receptor. Biochem. Biophys. Res. Commun. 235 (1997) 499-504
4. Beppu H., Kawabata M., Hamamoto T., Chytil A., Minowa O., Noda T., and Miyazono K. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev. Biol. 221 (2000) 249-258
5. Bisgrove B.W., Essner J.J., and Yost H.J. Regulation of midline development by antagonism of lefty and nodal signaling. Development 126 (1999) 3253-3262
6. Bisgrove B.W., Snarr B.S., Emrazian A., and Yost H.J. Polaris and Polycystin-2 in dorsal forerunner cells and Kupffer's vesicle are required for specification of the zebrafish left-right axis. Dev. Biol. 287 (2005) 274-288
7. Branford W.W., Essner J.J., and Yost H.J. Regulation of gut and heart left-right asymmetry by context-dependent interactions between xenopus lefty and BMP4 signaling. Dev. Biol. 223 (2000) 291-306
8. Carcamo J., Weis F.M., Ventura F., Wieser R., Wrana J.L., Attisano L., and Massague J. Type I receptors specify growth-inhibitory and transcriptional responses to transforming growth factor beta and activin. Mol. Cell. Biol. 14 (1994) 3810-3821
9. Chang H., Zwijsen A., Vogel H., Huylebroeck D., and Matzuk M.M. Smad5 is essential for left-right asymmetry in mice. Dev. Biol. 219 (2000) 71-78
10. Chang W., Parra M., Ji C., Liu Y., Eickelberg O., McCarthy T.L., and Centrella M. Transcriptional and post-transcriptional regulation of transforming growth factor beta type II receptor expression in osteoblasts. Gene 299 (2002) 65-77
11. Chen J.N., van Eeden F.J., Warren K.S., Chin A., Nusslein-Volhard C., Haffter P., and Fishman M.C. Left-right pattern of cardiac BMP4 may drive asymmetry of the heart in zebrafish. Development 124 (1997) 4373-4382
12. Chin A.J., Tsang M., and Weinberg E.S. Heart and gut chiralities are controlled independently from initial heart position in the developing zebrafish. Dev. Biol. 227 (2000) 403-421
13. Chocron S., Verhoeven M.C., Rentzsch F., Hammerschmidt M., and Bakkers J. Zebrafish Bmp4 regulates left-right asymmetry at two distinct developmental time points. Dev. Biol. 305 (2007) 577-588
14. Detrich III H.W., Kieran M.W., Chan F.Y., Barone L.M., Yee K., Rundstadler J.A., Pratt S., Ransom D., and Zon L.I. Intraembryonic hematopoietic cell migration during vertebrate development. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 10713-10717
15. Essner J.J., Branford W.W., Zhang J., and Yost H.J. Mesendoderm and left-right brain, heart and gut development are differentially regulated by pitx2 isoforms. Development 127 (2000) 1081-1093
16. Essner J.J., Amack J.D., Nyholm M.K., Harris E.B., and Yost H.J. Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 132 (2005) 1247-1260
17. Frisch A., and Wright C.V. XBMPRII, a novel Xenopus type II receptor mediating BMP signaling in embryonic tissues. Development 125 (1998) 431-442
18. Fujiwara T., Dehart D.B., Sulik K.K., and Hogan B.L. Distinct requirements for extra-embryonic and embryonic bone morphogenetic protein 4 in the formation of the node and primitive streak and coordination of left-right asymmetry in the mouse. Development 129 (2002) 4685-4696
19. Garg R.R., Bally-Cuif L., Lee S.E., Gong Z., Ni X., Hew C.L., and Peng C. Cloning of zebrafish activin type IIB receptor (ActRIIB) cDNA and mRNA expression of ActRIIB in embryos and adult tissues. Mol. Cell Endocrinol. 153 (1999) 169-181
20. Graff J.M., Thies R.S., Song J.J., Celeste A.J., and Melton D.A. Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 79 (1994) 169-179
21. Hamada H., Meno C., Watanabe D., and Saijoh Y. Establishment of vertebrate left-right asymmetry. Nat. Rev., Genet. 3 (2002) 103-113
22. Hashimoto H., Rebagliati M., Ahmad N., Muraoka O., Kurokawa T., Hibi M., and Suzuki T. The Cerberus/Dan-family protein Charon is a negative regulator of Nodal signaling during left-right patterning in zebrafish. Development 131 (2004) 1741-1753
23. Hassel S., Schmitt S., Hartung A., Roth M., Nohe A., Petersen N., Ehrlich M., Henis Y.I., Sebald W., and Knaus P. Initiation of Smad-dependent and Smad-independent signaling via distinct BMP-receptor complexes. J. Bone Joint Surg. Am. 85-A Suppl. 3 (2003) 44-51
24. Heldin C.H., Miyazono K., and ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390 (1997) 465-471
25. Hild M., Dick A., Bauer H., Schulte-Merker S., Haffter P., Bouwmeester T., and Hammerschmidt M. The roles of BMPs, BMP antagonists, and the BMP signaling transducers Smad1 and Smad5 during dorsoventral patterning of the zebrafish embryo. Ernst. Schering Res. Found. (2000) 81-106
26. Ishikawa T., Yoshioka H., Ohuchi H., Noji S., and Nohno T. Truncated type II receptor for BMP-4 induces secondary axial structures in Xenopus embryos. Biochem. Biophys. Res. Commun. 216 (1995) 26-33
27. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., and Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995) 253-310
28. Kishigami S., and Mishina Y. BMP signaling and early embryonic patterning. Cytokine Growth Factor Rev. 16 (2005) 265-278
29. Kishigami S., Yoshikawa S., Castranio T., Okazaki K., Furuta Y., and Mishina Y. BMP signaling through ACVRI is required for left-right patterning in the early mouse embryo. Dev. Biol. 276 (2004) 185-193
30. Kishimoto Y., Lee K.H., Zon L., Hammerschmidt M., and Schulte-Merker S. The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development 124 (1997) 4457-4466
31. Korchynskyi O., and ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J. Biol. Chem. 277 (2002) 4883-4891
32. Levin M. Left-right asymmetry in embryonic development: a comprehensive review. Mech. Dev. 122 (2005) 3-25
33. Liu F., Ventura F., Doody J., and Massague J. Human type II receptor for bone morphogenic proteins (BMPs): extension of the two-kinase receptor model to the BMPs. Mol. Cell. Biol. 15 (1995) 3479-3486
34. Long S., Ahmad N., and Rebagliati M. The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development 130 (2003) 2303-2316
35. Massague J., and Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J. 19 (2000) 1745-1754
36. Monteiro R.M., de Sousa Lopes S.M., Korchynskyi O., ten Dijke P., and Mummery C.L. Spatio-temporal activation of Smad1 and Smad5 in vivo: monitoring transcriptional activity of Smad proteins. J. Cell. Sci. 117 (2004) 4653-4663
37. Moustakas A., Souchelnytskyi S., and Heldin C.H. Smad regulation in TGF-beta signal transduction. J. Cell. Sci. 114 (2001) 4359-4369
38. Mullins M.C., Hammerschmidt M., Kane D.A., Odenthal J., Brand M., van Eeden F.J., Furutani-Seiki M., Granato M., Haffter P., Heisenberg C.P., Jiang Y.J., Kelsh R.N., and Nusslein-Volhard C. Genes establishing dorsoventral pattern formation in the zebrafish embryo: the ventral specifying genes. Development 123 (1996) 81-93
39. Nagaso H., Suzuki A., Tada M., and Ueno N. Dual specificity of activin type II receptor ActRIIb in dorso-ventral patterning during zebrafish embryogenesis. Dev. Growth Differ. 41 (1999) 119-133
40. Nakamura T., Mine N., Nakaguchi E., Mochizuki A., Yamamoto M., Yashiro K., Meno C., and Hamada H. Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition system. Dev. Cell 11 (2006) 495-504
41. Neave B., Holder N., and Patient R. A graded response to BMP-4 spatially coordinates patterning of the mesoderm and ectoderm in the zebrafish. Mech. Dev. 62 (1997) 183-195
42. Nishimatsu S., Suzuki A., Shoda A., Murakami K., and Ueno N. Genes for bone morphogenetic proteins are differentially transcribed in early amphibian embryos. Biochem. Biophys. Res. Commun. 186 (1992) 1487-1495
43. Nohno T., Ishikawa T., Saito T., Hosokawa K., Noji S., Wolsing D.H., and 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) 22522-22526
44. Odenthal J., and Nusslein-Volhard C. fork head domain genes in zebrafish. Dev. Genes Evol. 208 (1998) 245-258
45. Pfeffer P.L., Gerster T., Lun K., Brand M., and Busslinger M. Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2.1 (noi) function. Development 125 (1998) 3063-3074
46. Piedra M.E., and Ros M.A. BMP signaling positively regulates Nodal expression during left right specification in the chick embryo. Development 129 (2002) 3431-3440
47. Pyati U.J., Webb A.E., and Kimelman D. Transgenic zebrafish reveal stage-specific roles for Bmp signaling in ventral and posterior mesoderm development. Development 132 (2005) 2333-2343
48. Pyati U.J., Cooper M.S., Davidson A.J., Nechiporuk A., and Kimelman D. Sustained Bmp signaling is essential for cloaca development in zebrafish. Development 133 (2006) 2275-2284
49. Raya A., and Belmonte J.C. Left-right asymmetry in the vertebrate embryo: from early information to higher-level integration. Nat. Rev., Genet. 7 (2006) 283-293
50. Reiter J.F., Alexander J., Rodaway A., Yelon D., Patient R., Holder N., and Stainier D.Y. Gata5 is required for the development of the heart and endoderm in zebrafish. Genes Dev. 13 (1999) 2983-2995
51. Rodriguez Esteban C., Capdevila J., Economides A.N., Pascual J., Ortiz A., and Izpisua Belmonte J.C. The novel Cer-like protein Caronte mediates the establishment of embryonic left-right asymmetry. Nature 401 (1999) 243-251
52. Rosenzweig B.L., Imamura T., Okadome T., Cox G.N., Yamashita H., ten Dijke P., Heldin C.H., and Miyazono K. Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 7632-7636
53. Sakuma R., Ohnishi Yi Y., Meno C., Fujii H., Juan H., Takeuchi J., Ogura T., Li E., Miyazono K., and Hamada H. Inhibition of Nodal signalling by Lefty mediated through interaction with common receptors and efficient diffusion. Genes Cells 7 (2002) 401-412
54. Schilling T.F., Concordet J.P., and Ingham P.W. Regulation of left-right asymmetries in the zebrafish by Shh and BMP4. Dev. Biol. 210 (1999) 277-287
55. Schlange T., Arnold H.H., and Brand T. BMP2 is a positive regulator of Nodal signaling during left-right axis formation in the chicken embryo. Development 129 (2002) 3421-3429
56. Schottenfeld J., Sullivan-Brown J., and Burdine R.D. Zebrafish curly up encodes a Pkd2 ortholog that restricts left-side-specific expression of southpaw. Development 134 (2007) 1605-1615
57. Schulte-Merker S., van Eeden F.J., Halpern M.E., Kimmel C.B., and Nusslein-Volhard C. no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. Development 120 (1994) 1009-1015
58. Shen M.M. Nodal signaling: developmental roles and regulation. Development 134 (2007) 1023-1034
59. ten Dijke P., Yamashita H., Sampath T.K., Reddi A.H., Estevez M., Riddle D.L., Ichijo H., Heldin C.H., and Miyazono K. Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J. Biol. Chem. 269 (1994) 16985-16988
60. ten Dijke P., Korchynskyi O., Valdimarsdottir G., and Goumans M.J. Controlling cell fate by bone morphogenetic protein receptors. Mol. Cell. Endocrinol. 211 (2003) 105-113
61. Thisse C., Thisse B., Schilling T.F., and Postlethwait J.H. Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119 (1993) 1203-1215
62. Weinberg E.S., Allende M.L., Kelly C.S., Abdelhamid A., Murakami T., Andermann P., Doerre O.G., Grunwald D.J., and Riggleman B. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development 122 (1996) 271-280
63. Westerfield M. The Zebrafish Book (1995), University of Oregon Press, Eugene
64. Yamashita H., ten Dijke P., Huylebroeck D., Sampath T.K., Andries M., Smith J.C., Heldin C.H., and Miyazono K. Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J. Cell Biol. 130 (1995) 217-226
65. Yelon D., Horne S.A., and Stainier D.Y. Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. 214 (1999) 23-37