Evidence for a role of Smad6 in chick cardiac development

Developmental Biology

Volumn 215, Issue 1, 1999, Pages 48-61

  Yamada, Miho ^a   Szendro, Pablo I ^b   Prokscha, Alexander ^b   Schwartz, Robert J ^a   Eichele, Gregor ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Bone morphogenetic protein; Cardiac development; Chick embryo; Inhibitory SMAD; Smad1; Smad6

Indexed keywords

BONE MORPHOGENETIC PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL TISSUE; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; HEART DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

ANIMALIA; GALLUS GALLUS; MAMMALIA; VERTEBRATA;

EID: 0033230136     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9419     Document Type: Article

References (89)

1. Afrakhte M., Morén A., Jossan S., Itoh S., Sampath K., Wetermark B., Heldin C.-H., Heldin N.-E., ten Dijke P. Induction of inhibitory Smad6 and Smad7 mRNA by TGF-β family members. BBRC. 249:1998;505-511.
2. Albrecht U., Eichele G., Helms J. A., Lu H.-C. Visualization of gene expression patterns by in situ hybridization. Molecular and Cellular Methods in Developmental Toxicology. 1997;CRC Press, New York. p. 23-48.
3. Andrée B., Duprez D., Vorbusch B., Arnold H.-H., Brand T. BMP-2 induces ectopic expression of cardiac lineage markers and interferes with somite formation in chicken embryos. Mech. Dev. 70:1998;119-131.
4. Angerer L. M., Angerer R. C. In situ hybridization to cellular RNA with radiolabelled RNA probes. Wilkinson D. G. In Situ Hybridization: A Practical Approach. 1992;15-32 Oxford Univ. Press, Oxford.
5. Azpiazu N., Frasch M. tinman and bagpipe: Two homeobox genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev. 7:1993;1325-1340.
6. Barnett J. V., Moustakas A., Lin W., Wang X.-F., Lin H. Y., Galper J. B., Maas R. L. Cloning and developmental expression of the chick type II and type III TGFβ receptors. Dev. Dyn. 199:1994;12-27.
7. Barth J., Ivarie R. Polyvinyl alcohol enhances detection of low abundance transcripts in early stage quail embryos in a nonradioactive whole mount in situ hybridization technique. BioTechniques. 17:1994;324-327.
8. Bellairs R., Osmond M. Heart, blood vessels and lymphatics. The Atlas of Chick Development. 1998;Academic Press, San Diego. p. 25-35.
9. Bhushan A., Chen Y., Vale W. Smad7 inhibits mesoderm formation and promotes neural cell fate in Xenopus embryos. Dev. Biol. 200:1998;260-268.
10. Bodmer R., Jan L. Y., Jan Y. N. A new homeobox-containing gene, msh-2, is transiently expressed early during mesoderm formation of Drosophila. Development. 110:1990;661-669.
11. Bodmer R. The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development. 118:1993;719-729.
12. Bolender D. L., Markwald R. R. Epithelial-mesenchymal transformation in chick atrio-ventricular cushion morphogenesis. SEM. III:1979;313-321.
13. Casellas R., Hemmati-Brivanlou A. Xenopus Smad7 inhibits both the Activin and BMP pathways and acts as a neural inducer. Dev. Biol. 198:1998;1-12.
14. Chang H., Huylebroeck D., Verschueren K., Guo Q., Mazuk M. M., Zwijsen A. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development. 126:1999;1631-1642.
15. Choy M., Armstrong M. T., Armstrong P. B. Transforming growth factor-β1 localized within the heart of the chick embryo. Anat. Embryol. 183:1991;345-352.
16. Colvin E. V. Cardiac embryology. Garson A. Jr., Bricker J. T., McNamara D. G. The Science and Practice of Pediatric Cardiology. 1990;71-108 Lea & Febiger, Malvern.
17. Dick A., Risau W., Drexler H. Expression of Smad1 and Smad2 during embryogenesis suggests a role in organ development. Dev. Dyn. 211:1998;293-305.
18. 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.
19. Ehrman L. A., Yutzey K. E. Lack of regulation in the heart forming region of avian embryos. Dev. Biol. 207:1999;163-175.
20. Eisenberg L. M., Markwald R. R. Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ. Res. 77:1995;1-6.
21. Francis P. H., Richardson M. K., Brickell P. M., Tickle C. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development. 120:1994;209-218.
22. Frasch M. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature. 374:1995;464-467.
23. Furuta Y., Hogan B. L. M. BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 12:1998;3764-3775.
24. Garcia-Martinez S., Schoenwolf G. Primitive-streak origin of the cardiovascular system in avian embryos. Dev. Biol. 159:1993;706-719.
25. Hamburger V., Hamilton H. L. A series of normal stages in the development of the chick embryo. J. Morphol. 38:1951;49-92.
26. Harvey R. P. NK-2 homeobox genes and heart development. Dev. Biol. 178:1996;203-216.
27. Hata A., Lagna G., Massagué J., Hemmati-Brivanlou A. Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad6 tumor suppressor. Genes Dev. 12:1998;186-197.
28. Hayashi H., Abdollah S., Qui Y., Cai J., Xu Y.-Y., Grinnell B. W., Richardson M. A., Topper J. N., Gimbrone M. A. Jr., Wrana J. L., Falb D. The MAD-related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell. 89:1997;1165-1173.
29. Heldin C.-H., Miyazono K., ten Dijke P. TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature. 390:1997;465-471.
30. Hogan B. L. M. Bone morphogenic proteins: Multifunctional regulators of vertebrate development. Genes Dev. 10:1996;1580-1594.
31. Imamura T., Takase M., Nishihara A., Oeda E., Hanai J., Kawabata M., Miyazono K. Smad6 inhibits signalling by the TGF-β superfamily. Nature. 389:1997;622-626.
32. Jacobson A. G. Influences of ectoderm and endoderm on heart differentiation on the newt. Dev. Biol. 2:1960;138-154.
33. Jacobson A. G., Sater A. K. Features of embryonic induction. Development. 104:1988;341-359.
34. Jones C. M., Lyons K. M., Hogan B. L. M. Involvement of Bone Morphogenic Protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development. 111:1991;531-542.
35. Keyes W. M., Sanders E. J. Cell death in the endocardiac cushions of the developing heart. J. Mol. Cell. Cardiol. 31:1999;1015-1023.
36. Kleef J., Maruyama H., Friess H., Büchler M. W., Falb D., Korc M. Smad6 suppresses TGF-β-induced growth inhibition in COLO-357 pancreatic cancer cells and is overexpressed in pancreatic cancer. BBRC. 255:1999;268-273.
37. Kretzschmar M., Liu F., Hata A., Doody J., Massagué J. The TGF-β family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11:1997;984-995.
38. Kretzschmar M., Massagué J. SMADs: Mediators and regulators of TGF-β signaling. Curr. Opin. Genet. Dev. 8:1998;103-111.
39. Krug E. L., Mjaatvedt C. H., Markwald R. R. Extracellular matrix from embryonic myocardium elicits an early morphogenetic event in cardiac endothelial differentiation. Dev. Biol. 120:1987;348-355.
40. Lagna G., Hata A., Hemmati-Brivanlou A., Massague J. Partnership between DPC4 and SMAD proteins in TGFβ signalling pathways. Nature. 383:1996;832-836.
41. Lamb T. M., Knecht A. K., Smith W. C., Stachel S. E., Economides A. N., Stahl N., Yancopolous G. D., Harland R. M. Neural induction by the secreted polypeptide noggin. Science. 262:1993;713-718.
42. LeSueur J. A., Graff J. M. Spemann organizer activity of Smad10. Development. 126:1999;137-146.
43. Liu F., Hata A., Baker J. C., Doody J., Cárcamo J., Harland R. M., Massagué J. A human Mad protein acting as a BMP-regulated transcriptional activator. Nature. 381:1996;620-623.
44. 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.
45. Lyons K. M., 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.
46. Lyons I., Parsons L. M., Hartley L., Li R., Andrews J. E., Robb L., Harvey R. P. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev. 9:1995;1654-1666.
47. Macias-Silva M., Abdollah S., Hoodless P. A., Pirone R., Attisano L., Wrana J. L. MADR2 is a substrate of the TGFβ receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell. 87:1996;1215-1224.
48. Mai M., Grab R., Barnes R. D., Vafiadis P., Polychronakos C. Shortened PCR cycles in a conventional thermal cycler. BioTechniques. 25:1998;208-2110.
49. Markwald R. R., Mjaatvedt C. H., Krug E. L., Sinning A. R. Inductive interactions in heart development: role of cardiac adherons in cushion tissue formation. Ann. N.Y. Acad. Sci. 588:1990;13-25.
50. Mishina Y., Suzuki A., Ueno N., Behringer R. R. Bmpr encodes a type I bone morphogenic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 9:1995;3027-3037.
51. Nakajima Y., Krug E. L., Markwald R. R. Myocardial regulation of transforming growth factor-β expression by outflow tract endothelium in the early embryonic chick heart. Dev. Biol. 165:1994;615-626.
52. Nakajima Y., Yamagishi T., Nakamura H., Markwald R. R., Krug E. L. An autocrine function for transforming growth factor (TGF)-β3 in the transformation of atrioventricular canal endocardium into mesenchyme during chick heart development. Dev. Biol. 194:1998;99-113.
53. Nakao A., Afrakhte M., Morén A., Nakayama T., Christian J. L., Heuchel R., Itoh S., Kawabata M., Heldin N.-E., Heldin C.-H., ten Dijke P. Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature. 389:1997;631-635.
54. Nakayama T., Gardner H., Berg L. K., Christian J. L. Smad6 functions as an intracellular antagonist of some TGF-β family members during Xenopus embryogenesis. Genes Cells. 3:1998a;387-394.
55. Nakayama T., Snyder M. A., Grewal S. S., Tsuneizumi K., Tabata T., Christian J. L. Xenopus Smad8 acts downstream of BMP-4 to modulate its activity during vertebrate embryonic patterning. Development. 135:1998b;857-867.
56. Nascone N., Mercola M. An inductive role for the endoderm in Xenopus cardiogenesis. Development. 121:1995;515-523.
57. Nomura M., Li E. Smad2 role in mesoderm formation, left-right patterning and craniofacial development. Nature. 393:1998;786-790.
58. Oh S. H., Johnson R. L., Wu D. K. Differential expression of bone morphogenetic proteins in the developing vestibular and auditory sensory organs. J. Neurosci. 16:1996;6463-6475.
59. Ramsdell A. F., Markwald R. R. Induction of endocardial cushion tissue in the avian heart is regulated, in part, by TGFβ-3-mediated autocrine signaling. Dev. Biol. 188:1997;64-74.
60. Reecy J. M., Li X., Yamada M., DeMayo F. J., Newman C. S., Harvey R. P., Schwartz R. J. Identification of upstream regulatory regions in the heart-expressed homeobox gene Nkx2-5. Development. 126:1999;839-849.
61. Roberts D. J., Johnson R. L., Burke A. C., Nelson C. E., Morgan B. A., Tabin C. Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development. 121:1995;3163-3174.
62. Rosenquist G. C., DeHaan R. L. Migration of pancreatic cells in the chick embryo: A radioautographic study. Cardegie Inst. Wash. Publ. 625, Contributions Embryol. 263:1966;113-121.
63. Schultheiss T. M., Xydas S., Lassar A. B. Induction of avian cardiac myogenesis by anterior endoderm. Development. 121:1995;4203-4214.
64. Schultheiss T. M., Burch J. B. E., Lassar A. B. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 11:1997;451-462.
65. Selleck M. A., García-Castro M. I., Artinger K. B., Bronner-Fraser M. Effects of Shh and Noggin on neural crest formation demonstrate that BMP is required in the neural tube but not ectoderm. Development. 125:1998;4919-4930.
66. Sirard C., de la Pompa J. L., Elia A., Itie A., Mirtsos C., Cheung A., Hahn S., Wakeham A., Schwarta L., Kern S. E., Rossant J., Mak T. W. The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development. Genes Dev. 12:1998;107-119.
67. Solursh M., Langille R. M., Wood J., Sampath T. K. Osteogenic Protein-1 is required for mammalian eye development. BBRC. 218:1996;438-443.
68. Sugi Y., Sasse J., Lough J. Inhibition of precardiac mesoderm cell proliferation by antisense oligodeoxynucleotide complementary to fibroblast growth factor-2 (FGF-2). Dev. Biol. 157:1993;28-37.
69. Sugi Y., Lough J. Anterior endoderm is a specific effector of terminal cardiac myocyte differentiation of cells from the embryonic heart forming region. Dev. Dyn. 200:1994;155-162.
70. Sundin O., Eichele G. An early marker of axial pattern in the chick embryo and its respecification by retinoic acid. Development. 114:1992;841-852.
71. Takase M., Imamura T., Sampath T. K., Takeda K., Ichijo H., Miyazono K., Kawabata M. Induction of Smad6 mRNA by bone morphogenic proteins. BBRC. 244:1998;26-29.
72. Tanaka M., Chen Z., Bartunkova S., Yamasaki N., Izumo S. The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development. Development. 126:1999;1269-1280.
73. Topper J. N., Cai J., Qiu Y., Anderson K. R., Xu Y.-Y., Deeds J. D., Feeley R., Gimeno C. J., Woolf E. A., Tayber O., Mays G. G., Sampson B. A., Schoen F. J., Gimbrone M. A. Jr., Falb D. Vascular MADs: Two novel MAD-related genes selectively inducible by flow in human vascular endothelium. Proc. Natl. Acad. Sci. USA. 94:1997;9314-9319.
74. Tsuneizumi K., Nakayama T., Kamoshida Y., Kornberg T. B., Christian J. L., Tabata T. Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature. 389:1997;627-631.
75. Waldrip W. R., Bikoff E. K., Hoodless P. A., Wrana J. L., Robertson E. J. Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell. 92:1998;797-808.
76. Wawersik S., Purcell P., Rauchman M., Dudley A. T., Robertson E. J., Maas R. BMP7 acts in murine lens placode development. Dev. Biol. 207:1999;176-188.
77. Weinstein M., Yang X., Li C., Xu X., Gotay J., Deng C.-X. Failure of egg cyclinder elongation and mesoderm induction in mouse embryos lacking the tumor suppressor smad2. Proc. Natl. Acad. Sci. USA. 95:1998;9378-9383.
78. Whitman M. Feedback from inhibitory SMADs. Nature. 389:1997;549-551.
79. Whitman M. Smads and early developmental signaling by the TGF-β superfamily. Genes Dev. 12:1998;2445-2462.
80. 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.
81. Xu X., Yin Z., Hudson J. B., Ferguson E. L., Frasch M. Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev. 12:1998;2354-2370.
82. Yamagishi T., Nakajima Y., Sampath T. K., Miyazono K., Nakamura H. Bone morphogenetic protein 2 acts synergistically with transforming growth factor β3 in endothelial-mesenchymal cell transformation during chick heart development. Ann. N.Y. Acad. Sci. 857:1998;276-278.
83. Yang X., Li C., Xu X., Deng C. The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice. Proc. Natl. Acad. Sci. USA. 95:1998;3667-3672.
84. Yatskievych T. A., Ladd A. N., Antin P. B. Induction of cardiac myogenesis in avian pregastrula epiblast: The role of the hypoblast and activin. Development. 124:1997;2561-2570.
85. Zhang H., Bradley A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development. 122:1996;2977-2986.
86. Zhang Y., Feng X.-H., Wu R.-Y., Derynck R. Receptor-associated Mad homologues synergize as effectors of the TGF-β response. Nature. 383:1996;168-172.
87. Zhang Y., Musci T., Derynck R. The tumor suppressor Smad4/DPC4 as a central mediator of Smad function. Curr. Biol. 7:1997;270-276.
88. Zimmerman L. B., De Jesús-Escobar J. M., Harland R. M. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein4. Cell. 86:1996;599-606.
89. Zou H., Niswander L. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science. 272:1996;738-741.