Expression of smooth muscle alpha-actin in mesenchymal cells during formation of avian endocardial cushion tissue: A role for transforming growth factor β3

Developmental Dynamics

Volumn 209, Issue 3, 1997, Pages 296-309

  Nakajima, Yuji ^a,b   Mironov, Vladimir ^c   Yamagishi, Toshiyuki ^b   Nakamura, Hiroaki ^b   Markwald, Roger R ^a,c  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b SAITAMA MEDICAL UNIVERSITY   (Japan)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Avian embryo; Cardiogenesis; Endocardial cushion tissue; Smooth muscle alpha actin; TGF

Indexed keywords

ALPHA ACTIN; TRANSFORMING GROWTH FACTOR BETA3;

ANIMAL TISSUE; ARTICLE; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOSKELETON; EMBRYO DEVELOPMENT; HEART DEVELOPMENT; IMMUNOHISTOCHEMISTRY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL;

ACTINS; ANIMALS; ANTIBODIES, MONOCLONAL; CELLS, CULTURED; CHICK EMBRYO; ENDOCARDIUM; ENDOTHELIUM; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IMMUNOBLOTTING; ISOMERISM; MESODERM; MUSCLE, SMOOTH; STAINING AND LABELING; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; AVES; GALLUS GALLUS;

EID: 0031011870     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(199707)209:3<296::AID-AJA5>3.0.CO;2-D     Document Type: Article

References (63)

1. Akhurst, R.J. (1994) The transforming growth factor β family in vertebrate embryogenesis. In: "Growth Factors and Signal Transduction in Development." Nilsen-Hamilton, M. (ed). New York: Wiley-Liss, pp 97-122.
2. Arciniegas, E., Sutton, A.B., Allen, T.D., and Schor, A.M. (1992) Transforming growth factor beta 1 promotes the differentiation of endothelial cells into smooth muscle-like in vivo. J. Cell. Science 103:521-529.
3. Asashima, M., Nakano, H., Shimada, K., Kinoshita, K., Ishii, K., and Ueno, N. (1990) Mesodermal induction in early amphibian embryos by activin A (erythroid differentiation factor). Roux's Arch. Dev. Biol. 198:330-335.
4. Bains, W., Ponte, P., Blau, H., and Kedes, L. (1984) Cardiac actin is the major actin gene product in skeletal muscle cell differentiation in vitro. Mol. Cell. Biol. 4:1449-1453.
5. Bairati, A., and DeBiasi, S. (1981) Presence of a smooth muscle system in aortic valve leaflets. Anat. Embryol. 161:329-340.
6. Bernanke, D.H., and Markwald, R.R. (1982) Migratory behavior of cardiac cushion tissue cells in a collagen-lattice culture system. Dev. Biol. 91:235-245.
7. Brown, C.B., Boyer, A.S., Runyan, R.B., and Barnett, J.V. (1996) Antibodies to the type II TGFβ receptor block cell activation and migration during atrioventricular cushion transformation in the heart. Dev. Biol. 174:248-257.
8. Carroll, S.L., Bergsma, D.J., and Schwartz, R.J. (1986) Structure and complete nucleotide sequence of the chicken α-smooth muscle (aortic) actin gene. J. Biol. Chem. 261:8965-8976.
9. Carroll, S.L., Bergsma, D.J., and Schwartz, R.J. (1988) A29-nucleotide DNA segment containing an evolutionarily conserved motif is required in cis for cell-type-restricted repression of the chicken α-smooth muscle actin gene core promoter. Mol. Cell. Biol. 8:241-250.
10. Chang, K.S., Zimmer, W.E., Bergsma, D.J., Dodgson, J.B., and Schwartz, R.J. (1984) Isolation and characterization of six different chicken actin genes. Mol. Cell. Biol. 4:2498-2508.
11. Choy, M., Armstrong, M.T., and Armstrong, P.B. (1991) Transforming growth factor-β1 localized within the heart of the chick embryo. Anat. Embryol. 183:345-352.
12. Coffin, J.D., and Poole, T.J. (1988) Embryonic vascular development: immunohistochemical identification of the origin and subsequent morphogenesis of the major vessel primordia in quail embryos. Development 102:735-784.
13. Coffin, J.D., and Poole, T.J. (1991) Endothelial cell origin and migration in embryonic heart and cranial blood vessel development. Anat. Rec. 231:383-395.
14. Crossin, K.C., and Hoffman, S. (1991) Expression of adhesion molecules during the formation and differentiation of the avian endocardial cushion tissue. Dev. Biol. 145:277-286.
15. Crossley, P.H., Minowada, G., MacArthur, C.A., and Martin, G.R. (1996) Roles for FGF8 in the induction, initiation, and maintenance of chick limb development. Cell 84:127-136.
16. Davis, C.L. (1927) Development of the human heart from its first appearance to the stage found in embryos of twenty paired somites. Contrib. Embryol. 19:245-284.
17. De La Cruz, M.V., Sanchez-Gomez, C., and Palomino, M.A. (1989) The primitive cardiac regions in the straight tube heart (stage 9 ) and their anatomical expression in the mature heart: An experimental study in the chick embryo. J. Anat. 165:121-131.
18. Desmouliere, A., Geinoz, A., Gabbiani, F., and Gabbiani, G. (1993) Transforming growth factor-β1 induces α-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblast. J. Cell. Biol. 122:103-111.
19. Eisenberg, L.M., and Markwald, R.R. (1995) Molecular regulation of atrioventricular valvulospetal morphogenesis. Circ. Res. 77:1-6.
20. Fallon, J.F., Lopez, A., Ros, M.A., Savage, M.P., Olwin, B.B., and Simandl, B.K. (1994) FGF-2: Apical ectodermal ridge growth signal for chick limb development. Science 264:104-107.
21. Filip, D.A., Radu, A., and Simionescu, A. (1986) Interstitial cells of the heart valve possess characteristics similar to smooth muscle cells. Circ. Res. 59:310-319.
22. Funderburg, F.M. and Markwald, R.R. (1986) Conditioning of native substrates by chondroitin sulfate proteoglycans during cardiac mesenchymal cell migration. J. Cell. Biol. 103:2475-2487.
23. Gabbiani, G., Ryan, G.B., and Majno, G. (1971) Presence of modified fibroblasts in granulation tissue and their possible role in wound contraction. Experientia 27:549-550.
24. Gurdon, J.B., Fairman, S., Mohun, T.J. and Brennan, S. (1985) Activation of muscle-specific actin genes in Xenopus development by an induction between animal and vegetal cells of a blastula. Cell 41:913-922.
25. Hamburger, V., and Hamilton, H. L. (1951) A series of normal stages in the development of the chick embryo. J. Morphol. 88:49-92.
26. Kimelman, D., and Kirschner, M.W. (1987) Synergistic induction of mesoderm by FGF and TGFβ and identification of an mRNA coding for FGF in the early Xenopus embryo. Cell 51:869-877.
27. Kirby, M.L., Gale, T.F., and Stewart, D.E. (1983) Neural crest cells contribute to normal aorticopulmonary septation. Science 220:1059-1061.
28. Kocher, O., and Gabbiani, G. (1987) Analysis of α-smooth muscle actin mRNA expression in rat aortic smooth-muscle cells using a specific cDNAprobe. Differentiation 34:201-209.
29. Krug, E.L., Mjaatvedt, C.H., and Markwald, R.R. (1987) Extracellular matrix from embryonic myocardium elicits an early morphogenetic event in cardiac endothelial differentiation. Dev. Biol. 120:348-355.
30. Krug, E.L., Rezaee, M., Isokawa, K., Turner, D.K., Litke, L.L., Wunsch, A.M., Bain, J.L., Riley, D.A., Capehart, A.A., and Markwald, R.R. (1995) Transformation of cardiac endocardium into cushion mesenchyme is dependent on ES/130: Temporal, spatial, and functional studies in the early chick embryo. Cell. Mol. Biol. Res. 41:263-277.
31. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the heard of bacteriophage T4. Nature 227:680-685.
32. Markwald, R.R., Fitzharris, T.P., and Adams-Smith, W.N. (1975) Structural analysis of endocardial cytodifferentiation. Dev. Biol. 42:160-180.
33. Markwald, R.R., Fitzharris, T.P., and Manasek, F.J. (1977) Structural development of endocardial cushions. Amer. J. Anat. 148:85-120.
34. McGuire, P.G., and Orkin, R.W. (1992) Urokinase activity in the developing avian heart: A spatial and temporal analysis. Dev. Dyn. 193:24-33.
35. McHugh, K.M., Crawford, K., and Lessard, J.L. (1991) A comprehensive analysis of the development and tissue-specific expression of the isoactin multigene family in the rat. Dev. Biol. 148:442-458.
36. Mironov, V.A., Hill, C.H., Starcher, B., Shih, J., Hoffman, S., and Markwald, R.R. (1995) Endothelial mesenchymal transformation in atherosclerosis: A recapituration of embryonic heart cushion morphogenesis. Ann. Biomed. Engineer. 23:S-29A.
37. Mjaatvedt, C.H., and Markwald, R.R. (1989) Induction of an epithelial mesenchymal transition by an in vivo adheron-like complex. Dev. Biol. 136:118-128.
38. Mjaatvedt, C.H., Krug, E.L., and Markwald, R.R. (1991) An antiserum (ES1) against a particulate form of extracellular matrix blocks the transition of cardiac endothelium into mesenchyme in culture. Dev. Biol. 145:219-230.
39. Nakajima, Y., Krug, E.L., and Markwald, R.R. (1994) Myocardial regulation of transforming growth factor-β expression by outflow tract endothelium in the early embryonic chick heart. Dev. Biol. 165:615-626.
40. Noden, D.M. (1991) Origin and patterning of avian outflow tract endocardium. Development 111:867-876.
41. Pardanaud, L., Altmann, C., Kitos, P., Dieterlen-Lievre, F., and Buck, C.A. (1987) Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100:339-349.
42. Pardanaud, L., Yassine, F., and Dieterlen-Lievre, F. (1989) Relationship between vasculogenesis, angiogenesis and haemopoiesis during avian ontogeny. Development 105:473-485.
43. Potts, J.D., and Runyan, R.B. (1989) Epithelial-mesenchymal cell transformation in the embryonic heart can be mediated, in part, by transforming growth factor β. Dev. Biol. 134:392-401.
44. Potts, J.D., Dagle, J.M., Walder, J.A., Weeks, D.J., and Runyan, R.B. (1991) Epithelial-mesenchymal transformation of embryonic endothelial cells is inhibited by a modified antisense oligodeoxynucleotide to transforming growth factor β. Proc. Natl. Acad. Sci. USA 88:1516-1520.
45. Risau, W. (1995) Differentiation of endothelium. FASEB J. 9:926-933.
46. Ross, R. (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362:801-809.
47. Runyan, R.B., Potts, J.D., and Weeks, D.L. (1992) TGF-β3-mediated tissue interaction during embryonic heart development. Mol. Reprod. Dev. 32:152-159.
48. Ruzicka, D.L., and Schwartz, R. (1988) Sequential activation of α-actin genes during avian cardiogenesis: Vascular smooth muscle α-actin gene transcripts mark the onset of cardiomyocyte differentiation. J. Cell Biol. 107:2575-2586.
49. Saint-Jeannet, J-P., Levi, G., Girault, J-M., Koteliansky, V., and Thiery, J-P. (1992) Ventrolateral regionalization of Xenopus laevis mesoderm is characterized by the expression of α-smooth muscle actin. Development 115:1165-1173.
50. Skalli, O., Ropraz, P., Trzeciak, A., Benzonana, G., Gillessen, D., and Gabbiani, G. (1986) A monoclonal antibody against α-smooth muscle actin: A new probe for smooth muscle differentiation. J. Cell. Biol. 103:2787-2796.
51. Slack, J.M.W., Darlington, B.G., Health, J.K., and Godsave, S.F. (1987) Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. Nature 326:197-200.
52. Spemann, H. (1938) "Embryonic Development and Induction." New Haven: Yale University Press.
53. Sugi, Y., and Lough, J. (1992) Onset of expression and regional deposition of alpha-smooth and sarcomeric actin during avian heart development. Dev. Dyn. 193:116-124.
54. Sugi, Y., Sasse, J., and Lough, J. (1993) Inhibition of precardiac mesoderm cell proliferation by antisense oligodeoxynucleotide complementary to fibroblast growth factor-2 (FGF-2). Dev. Biol. 157:28-37.
55. Sugi, Y., and Markwald, R.R. (1996) Formation and early morphogenesis of endocardial endothelial precursor cells and the role of endoderm. Dev. Biol. 175:66-83.
56. Sumida, H., Akimoto, N., and Nakamura, H. (1989) Distribution of the neural crest cells in the heart of birds: a three dimensional analysis. Anat. Embryol. 180:29-35.
57. Vandekerckhove, J., and Weber, K. (1978) At least six different actins are expressed in a higher mammal: an analysis based on the amino acid sequence of the ammo-terminal tryptic peptide. J. Mol. Biol. 126:783-802.
58. Vandekerckhove, J., and Weber, K. (1981) Actin typing on total cellular extracts. A highly sensitive protein-chemical procedure able to distinguish actins. Eur. J. Biochem. 113:595-603.
59. Vandekerckhove, J., Bugaisky, B., and Buckingham, M. (1986) Simultaneous expression of skeletal muscle and heart actin proteins in various striated muscle tissues and cells. J. Biol. Chem. 261:1838-1843.
60. Woodcock-Mitchell, J., Mitchell, J.J., Low, R.B., Kieny, M., Sengel, P., Rubbia, L., Skalli, O., Jackson, B., and Gabbiani, G. (1988) α-Smooth muscle actin is transiently expressed in embryonic rat cardiac and skeletal muscles. Differentiation 39:161-166.
61. Wunsch, A., Little, C.D., and Markwald, R.R. (1994) Cardiac endothelial heterogeneity is demonstrated by the diverse expression of JB3 antigen, a fibrillin-like protein of the endocardial cushion tissue. Dev. Biol. 165:585-601.
62. Yamazaki, Y., and Hirakow, R. (1991) Factors required for differentiation of chick precardiac mesoderm cultured in vitro. Proc. Jap. Acad. Sci. 67:165-169.
63. Yamazaki, Y., and Hirakow, R. (1994) Effect of growth factors on the differentiation of chick precardiac mesoderm in vitro. Roux's Dev. Biol. 203:290-294.