Role of The Cardiac Neural Crest in Outflow Tract of Heart

Sachiko Miyagawa-Tomita

doi:10.11276/jsvc1984.31.1

Sachiko Miyagawa-Tomita

Author information

Keywords: cardiac neural crest, heart anomaly, chick embryo, outflow tract, transcription factor

JOURNAL FREE ACCESS

1998 Volume 31 Issue 1 Pages 1-17

DOI https://doi.org/10.11276/jsvc1984.31.1

Details

Published: 1998 Received: - Available on J-STAGE: March 05, 2010 Accepted: - Advance online publication: - Revised: -
Correction information
Date of correction: March 05, 2010 Reason for correction: - Correction: AFFILIATION Details: Wrong :
1) Department of Pediatric Cardiology, the Heart Institute of Japan

Right :
1) Department of Pediatric Cardiology, the Heart Institute of Japan, Tokyo Women's Medical University

Date of correction: March 05, 2010 Reason for correction: - Correction: CITATION Details: Wrong : 2) Fukuishi, Y. and G.M. Morris-Kay(1992):Migration of cranial neural crest cells to the pharyngeal arches and heart in rat embryos. Cell Tissue. Res., 268, 1-8.
3) Kirby, M. L. (1995):Neural crest and cardiovascular patterning. Circ. Res., 77, 211-215.
4) Hamburger, V. and H. L. Hamilton (1951):A series of normal stages in development of the chick embryo. J. Morph., 88, 49-92.
5) Miyagawa-Tomita, S., Waldo, K., Tomita, H.and M.L. Kirby (1992):Temporospatial study of the migration and distribution of cardiac neural crest in quail-chick chimeras. Am. J. Anat., 192, 79-88.
6) Le Douarin, N. M.:The neural crest. Cambridge Univ. Press, Cambridge, Mass., 1984
8) Le Lievre, C. S. and N.M. Le Dourain (1975):Mesenchymal derivatives of the neural crest:analysis of chimeric quail and chick embryos. J. Embryol. Exp. Morphol., 34, 125-154.
9) Rychter, Z.:Analysis of relations between aortic arches and aorticopulmonary septation. In:Morphogenesis and malformation of the cardiovascular system, Rosenquist, G.C. and D. Bergsma ed, 14(7), pp.443-448, Alan R. Liss., New York, 1978.
10) Thompson, R. P. and T. P. Fitzharris (1979):Morphogenesis of the truncus arteriosus of the chick embryo heart:The formation and migration of mesenchymal tissue. Am. J. Anat., 154, 545-555.
11) Kirby, M. L., Gale, T. F. and D. E. Stewart (1983):Neural crest cells contribute to aorticopulmonary septation. Science, 220, 1059-1061.
12) Ikeya, M., Lee, S. M. K., Johnson, J.E., McMahon, A.P. and S. Takada (1997):Wnt signalling required for expansion of neural crest and CNS progenitors. Nature, 389,966-970.
13) McGinnis, W. and R. Krumlauf (1992):Homeobox genes and axial patterning. Cell, 68, 283-302.
14) Hunt, P., Gulisano, M., Cook, M., Sham, M., Faiella, A., Wilkinson, D., Boncinelli, E. and R. Krumlauf (1991):A distinct Hox code for the branchial region of the vertebrate head. Nature, 353, 861-864.
16) Chisaka, O. and M.R. Capecchi (1991):Regionally restricted developmental defects resulting from targeted disruption of the mouse homeobox gene hox-1.5. Nature, 350, 473-479.
17) Kirby, M.L., Hunt, P., Wallis, K. and P. Thorogood (1997):Abnormal patterning of the aortic arteries does not evoke cardiac malformations. Dev. Dyn., 208, 34-47.
18) Kirby, M.L. et al. (1990) Role of neural crest in congenital disease. Circulation, 82, 332-340
19) Nihsibatake, M., Kirby, M.L. and L.H.S., Van Mierop (1987):Pathogenesis of persistent truncus arteriosus and dextroposed aorta in the chick embryo after neural crest ablation. Circulation, 75(1), 255-264.
20) Kirby, M.L. (1989):Plasticity and predetermination of mesencepahlic and trunk neural crest transplanted into the region of the cardiac neural crest. Dev. Biol., 134, 402-412.
21) Kirby, M. L. (1988):Nodose placode provides ectomesenchyme to the developing chick heart in the absence of cardiac neural crest. Cell Tissue Res., 252, 17-22.
22) Iida, K., Koseki, H., Kakinuma, H., Kato, N., M-Koseki, Y., Ohuchi, H., Yoshioka, H., Noji, S., Kawamura, K., Kataoka, Y., Ueno, F., Taniguchi, M., Yoshida, N., Sugiyama, T. and N. Miura (1997):Essential roles of the winged helix transcription factor MFH-1 in aortic arch patterning and skeletogenesis. Development, 124, 4627-4638.
23) Yanagisawa, H., Yanagisawa, M., Kapur, R. P., Richardson, J. A., Williams, S. C., Clouthier, D. E., de Wit, D., Emoto, N. and R. E. Hammer (1998):Dual genetic pathway of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene. Development, 125, 825-836.
24) Kurihara, Y., Kurihara, H., Oda, H., Maemura, K., Nagai, R., Ishikawa, T. and Y. Yazaki (1996):Aortic arch malformations and ventricular septal defect in mice deficient in endothelin-1. J. Clin. Invest., 96, 293-300.
25) Clouthier, E.D., Hosoda, K., Richardson, J.A., Williams, S.C., Yanagisawa, H., Kuwaki, T., Kumada, M., Hammer, R.E. and M. Yanagisawa (1998):Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice. Development, 125, 813-824.
26) Franz, T. (1989):Persistent truncus arteriosus in the Splotch mutant mouse. Anat. Embryol., 180, 457-464.
27) Tassabehji, M., Read, A., Newton, V. E., Harris, R., Balling, R., Gruss, P. and T. Strachan (1993):Waardenburg's syndrome patients have mutations in the human homologue of the Pax-3 paired box gene. Nature, 355, 635-636.
28) Brannan, C. I., Perkins, A. S., Vogel, K. S., Ratner, N., Nordlund, M.L., Reid, S. W., Buchberg, A. M., Jenkins, N. A., Parada, L. F. and N.G. Copeland (1994):Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crestderived tissues. Genes Devel, 8, 1019-1029.
29) Jacks, T., Shih, T. S., Schmitt, E. M., Bronson, R. T., Bernards, A. and R. A. Weinberg (1994):Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nature Genet., 7, 353-361, 1994.
30) Lakkis, M. M. and J. A. Epstein (1998):Neurofibromin modulates ras mediated epithelial-mesenchymal transformation in the endocardial cushions. Weinstein Cardiovascular Development Conference, S21, abstract.
31) Sartin, E. A., Doran, S. E., Riddell, M. G., Herrera, G. A., Tennyson, G. S., D'Andrea, G., Whitley, R. D. and F. S. Collins (1994):Characterization of naturally occuring cutaneous neurofibromatosis in Holstein cattle. Am. J. Pathol., 145,1168-1174.
32) Schilham, M. W., Oosterwegel, M. A., Moerer, P., Ya, J., De Boer, P. A. J., Van de Wetering, M., Verbeek, S., Lamers, W. H., Kruisbeek, A.M., Cumano, A. and H. Clevers (1996):Defects in cardiac outflow tract formation and pro-Blymphocyte expansion in mice lacking Sox-4. Nature, 380, 711-714.
33) Lamers, W.H., Ya, J., Schilham, M. W., de Boer, P. A.. J., Moorman, A.F. M. and H. Clevers (1998):The Sox4-deficiency syndrome in mice is an animal model for common tunk. Weinstein Cardiovascular Development Conference, S30, abstract.
34) de la Pompa, J. L., Timmerman, L. A., Takimoto, H., Yoshida, H., Elia, A. J., Samper, E., Potter, J., Wakeham, A., Marengere, L., Langille, B. L., Crabtree, G. R. and T. W. Mak (1998):Role of the NF-ATc transcription factor in morphogenesis of cardiac valve and septum. Nature, 392, 182-186.
35) Ranger, A. M.,Grusby, M. J., Hodge, M. R., Gravallese, E. M., de la Brousse, F. C., Hoey, T., Mickanin, C., Baldwin, S. H. and L. H. Glimcher (1998):The transcription factor NF-ATc is essential for cardiac valve formation. Nature, 392, 186-190.
36) Wilson, D. I., Burn, J., Scambler, P. and J. Goodship (1993):DiGeorge syndrome:Part of CATCH 22. J. Med. Genet., 30, 852-856.
37) DiGeorge, A.M.:Congenital absence of the thymus and its immunologic consequence:Concurrence with congenital hypoparathyroidism. In:Im-munologic Deficiency Disease in man, Bergsma, D. and R. A. Good ed., OAS IV(1), pp.116, White Plains for the National Foundation-March of Dimes Academic Press, 1968.
39) Shprintzen, R. J., Goldberg, R. B., Lewin, M. L., Sidotim, E. J., Berkman, M. D., Argamaso, R. V. and D. Young (1978):A New syndrome involving cleft palate, cardiac anomalies, typical faces, and learning disabilities:Velo-cardio-facial syndrome. Cleft Palate J., 15, 56-62.
40) McDonald-McGinn, D. M., Driscoll, D. A., Bason, L., Christensen, C., Lynch, D., Sullivan, K., Canning, D., Zavod, W., Quinn, N., Rome, J., Paris, Y., Weinberg, P., Clark, B.J., Emanuel, B.S. and E. H. Zackai (1995):Autosomal dominant “OPITZ” GBBB syndrome due to a 22q11.2 deletion. Am. J. Med. Genet., 59, 103-113.

Right : 2) Fukuishi, Y. and G.M. Morris-Kay(1992):Migration of cranial neural crest cells to the pharyngeal arches and heart in rat embryos. Cell Tissue. Res., 268, 1-8.
3) Kirby, M. L. (1995):Neural crest and cardiovascular patterning. Circ. Res., 77, 211-215.
4) Hamburger, V. and H. L. Hamilton (1951):A series of normal stages in development of the chick embryo. J. Morph., 88, 49-92.
5) Miyagawa-Tomita, S., Waldo, K., Tomita, H.and M.L. Kirby (1992):Temporospatial study of the migration and distribution of cardiac neural crest in quail-chick chimeras. Am. J. Anat., 192, 79-88.
6) Le Douarin, N. M.:The neural crest. Cambridge Univ. Press, Cambridge, Mass., 1984
8) Le Lievre, C. S. and N.M. Le Dourain (1975):Mesenchymal derivatives of the neural crest:analysis of chimeric quail and chick embryos. J. Embryol. Exp. Morphol., 34, 125-154.
9) Rychter, Z.:Analysis of relations between aortic arches and aorticopulmonary septation. In:Morphogenesis and malformation of the cardiovascular system, Rosenquist, G.C. and D. Bergsma ed, 14(7), pp.443-448, Alan R. Liss., New York, 1978.
10) Thompson, R. P. and T. P. Fitzharris (1979):Morphogenesis of the truncus arteriosus of the chick embryo heart:The formation and migration of mesenchymal tissue. Am. J. Anat., 154, 545-555.
11) Kirby, M. L., Gale, T. F. and D. E. Stewart (1983):Neural crest cells contribute to aorticopulmonary septation. Science, 220, 1059-1061.
12) Ikeya, M., Lee, S. M. K., Johnson, J.E., McMahon, A.P. and S. Takada (1997):Wnt signalling required for expansion of neural crest and CNS progenitors. Nature, 389,966-970.
13) McGinnis, W. and R. Krumlauf (1992):Homeobox genes and axial patterning. Cell, 68, 283-302.
14) Hunt, P., Gulisano, M., Cook, M., Sham, M., Faiella, A., Wilkinson, D., Boncinelli, E. and R. Krumlauf (1991):A distinct Hox code for the branchial region of the vertebrate head. Nature, 353, 861-864.
16) Chisaka, O. and M.R. Capecchi (1991):Regionally restricted developmental defects resulting from targeted disruption of the mouse homeobox gene hox-1.5. Nature, 350, 473-479.
17) Kirby, M.L., Hunt, P., Wallis, K. and P. Thorogood (1997):Abnormal patterning of the aortic arteries does not evoke cardiac malformations. Dev. Dyn., 208, 34-47.
18) Kirby, M.L. et al. (1990) Role of neural crest in congenital disease. Circulation, 82, 332-340
19) Nihsibatake, M., Kirby, M.L. and L.H.S., Van Mierop (1987):Pathogenesis of persistent truncus arteriosus and dextroposed aorta in the chick embryo after neural crest ablation. Circulation, 75(1), 255-264.
20) Kirby, M.L. (1989):Plasticity and predetermination of mesencepahlic and trunk neural crest transplanted into the region of the cardiac neural crest. Dev. Biol., 134, 402-412.
21) Kirby, M. L. (1988):Nodose placode provides ectomesenchyme to the developing chick heart in the absence of cardiac neural crest. Cell Tissue Res., 252, 17-22.
22) Iida, K., Koseki, H., Kakinuma, H., Kato, N., M-Koseki, Y., Ohuchi, H., Yoshioka, H., Noji, S., Kawamura, K., Kataoka, Y., Ueno, F., Taniguchi, M., Yoshida, N., Sugiyama, T. and N. Miura (1997):Essential roles of the winged helix transcription factor MFH-1 in aortic arch patterning and skeletogenesis. Development, 124, 4627-4638.
23) Yanagisawa, H., Yanagisawa, M., Kapur, R. P., Richardson, J. A., Williams, S. C., Clouthier, D. E., de Wit, D., Emoto, N. and R. E. Hammer (1998):Dual genetic pathway of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene. Development, 125, 825-836.
24) Kurihara, Y., Kurihara, H., Oda, H., Maemura, K., Nagai, R., Ishikawa, T. and Y. Yazaki (1996):Aortic arch malformations and ventricular septal defect in mice deficient in endothelin-1. J. Clin. Invest., 96, 293-300.
25) Clouthier, E.D., Hosoda, K., Richardson, J.A., Williams, S.C., Yanagisawa, H., Kuwaki, T., Kumada, M., Hammer, R.E. and M. Yanagisawa (1998):Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice. Development, 125, 813-824.
26) Franz, T. (1989):Persistent truncus arteriosus in the Splotch mutant mouse. Anat. Embryol., 180, 457-464.
27) Tassabehji, M., Read, A., Newton, V. E., Harris, R., Balling, R., Gruss, P. and T. Strachan (1993):Waardenburg's syndrome patients have mutations in the human homologue of the Pax-3 paired box gene. Nature, 355, 635-636.
28) Brannan, C. I., Perkins, A. S., Vogel, K. S., Ratner, N., Nordlund, M.L., Reid, S. W., Buchberg, A. M., Jenkins, N. A., Parada, L. F. and N.G. Copeland (1994):Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crestderived tissues. Genes Devel, 8, 1019-1029.
29) Jacks, T., Shih, T. S., Schmitt, E. M., Bronson, R. T., Bernards, A. and R. A. Weinberg (1994):Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nature Genet., 7, 353-361, 1994.
30) Lakkis, M. M. and J. A. Epstein (1998):Neurofibromin modulates ras mediated epithelial-mesenchymal transformation in the endocardial cushions. Weinstein Cardiovascular Development Conference, S21, abstract.
31) Sartin, E. A., Doran, S. E., Riddell, M. G., Herrera, G. A., Tennyson, G. S., D'Andrea, G., Whitley, R. D. and F. S. Collins (1994):Characterization of naturally occuring cutaneous neurofibromatosis in Holstein cattle. Am. J. Pathol., 145,1168-1174.
32) Schilham, M. W., Oosterwegel, M. A., Moerer, P., Ya, J., De Boer, P. A. J., Van de Wetering, M., Verbeek, S., Lamers, W. H., Kruisbeek, A.M., Cumano, A. and H. Clevers (1996):Defects in cardiac outflow tract formation and pro-B-lymphocyte expansion in mice lacking Sox-4. Nature, 380, 711-714.
33) Lamers, W.H., Ya, J., Schilham, M. W., de Boer, P. A.. J., Moorman, A.F. M. and H. Clevers (1998):The Sox4-deficiency syndrome in mice is an animal model for common tunk. Weinstein Cardiovascular Development Conference, S30, abstract.
34) de la Pompa, J. L., Timmerman, L. A., Takimoto, H., Yoshida, H., Elia, A. J., Samper, E., Potter, J., Wakeham, A., Marengere, L., Langille, B. L., Crabtree, G. R. and T. W. Mak (1998):Role of the NF-ATc transcription factor in morphogenesis of cardiac valve and septum. Nature, 392, 182-186.
35) Ranger, A. M.,Grusby, M. J., Hodge, M. R., Gravallese, E. M., de la Brousse, F. C., Hoey, T., Mickanin, C., Baldwin, S. H. and L. H. Glimcher (1998):The transcription factor NF-ATc is essential for cardiac valve formation. Nature, 392, 186-190.
36) Wilson, D. I., Burn, J., Scambler, P. and J. Goodship (1993):DiGeorge syndrome:Part of CATCH 22. J. Med. Genet., 30, 852-856.
37) DiGeorge, A.M.:Congenital absence of the thymus and its immunologic consequence:Concurrence with congenital hypoparathyroidism. In:Im-munologic Deficiency Disease in man, Bergsma, D. and R. A. Good ed., OAS IV(1), pp.116, White Plains for the National Foundation-March of Dimes Academic Press, 1968.
39) Shprintzen, R. J., Goldberg, R. B., Lewin, M. L., Sidotim, E. J., Berkman, M. D., Argamaso, R. V. and D. Young (1978):A New syndrome involving cleft palate, cardiac anomalies, typical faces, and learning disabilities:Velo-cardio-facial syndrome. Cleft Palate J., 15, 56-62.
40) McDonald-McGinn, D. M., Driscoll, D. A., Bason, L., Christensen, C., Lynch, D., Sullivan, K., Canning, D., Zavod, W., Quinn, N., Rome, J., Paris, Y., Weinberg, P., Clark, B.J., Emanuel, B.S. and E. H. Zackai (1995):Autosomal dominant “OPITZ” GBBB syndrome due to a 22q11.2 deletion. Am. J. Med. Genet., 59, 103-113.

Abstract

Normal development of the heart and great arteries requires the contribution of the cardiac neural crest. Ectomesenchymal cells from this area of the neural crest migrate to pharyngeal arches 3, 4, and 6, where they support development of the aortic arch arteries and give rise to connective tissues. The cells continue their migration from the pharyngeal arches to specific sites in the outflow tract of the heart. Removal of the neural crest before migration results in two major types of malformations: truncal septation defects and aortic arch anomalies. Truncal septation is disturbed when the cells do not reach the outflow tract. Patterning of the aortic arch arteries is perturbed when the cells do not form connective tissue and tunica media to support the aortic arch arteries. With the advent of genetically based animal models with cardiovascular anomalies, some of which are neural crest related, it becomes important to understand what we know from ablation studies and which questions remain. Some possible molecular mechanisms involved in specifying the neural crest and/or outflow tract for participation in heart development are discussed.

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Correction information

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