Evolutionary and developmental origins of the cardiac neural crest: Building a divided outflow tract

Birth Defects Research Part C - Embryo Today: Reviews

Volumn 102, Issue 3, 2014, Pages 309-323

  Keyte, Anna L ^a   Alonzo Johnsen, Martha ^a   Hutson, Mary R ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac neural crest; Evolution; Outflow tract septation; Pharyngeal arch artery remodeling; Second heart field

Indexed keywords

ANIMAL; ANIMAL MODEL; BIRD; CARDIOVASCULAR SYSTEM; CYTOLOGY; EMBRYOLOGY; EVOLUTION; HUMAN; MAMMAL; NEURAL CREST;

ANIMALS; BIOLOGICAL EVOLUTION; BIRDS; CARDIOVASCULAR SYSTEM; HUMANS; MAMMALS; MODELS, ANIMAL; NEURAL CREST;

EID: 84908545042     PISSN: 1542975X     EISSN: 15429768     Source Type: Journal    
DOI: 10.1002/bdrc.21076     Document Type: Article

References (112)

1. Abu-Issa R, Smyth G, Smoak I, Yamamura K-I, Meyers EN. 2002. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 129:4613-4625.
2. Arima Y, Miyagawa-Tomita S, Maeda K, Asai R, et al. 2012. Preotic neural crest cells contribute to coronary artery smooth muscle involving endothelin signalling. Nat Commun 3:1267.
3. Ataliotis P, Ivins S, Mohun TJ, Scambler PJ. 2005. XTbx1 is a transcriptional activator involved in head and pharyngeal arch development in Xenopus laevis. Dev Dyn 232:979-991.
4. Bajolle F, Zaffran S, Meilhac SM, Dandonneau M, et al. 2008. Myocardium at the base of the aorta and pulmonary trunk is prefigured in the outflow tract of the heart and in subdomains of the second heart field. Dev Biol 313:25-34.
5. Bamforth SD, Chaudhry B, Bennett M, Wilson R, et al. 2013. Clarification of the identity of the mammalian fifth pharyngeal arch artery. Clin Anat 26:173-182.
6. Bemis EW, Burggren WW, Kemp NE, Zoologists ASO. 1987. The biology and evolution of lungfishes. New York: A.R. Liss.
7. Bergwerff M, Verberne ME, DeRuiter MC, Poelmann RE, et al. 1998. Neural crest cell contribution to the developing circulatory system: implications for vascular morphology? Circ Res 82:221-231.
8. Bertrand N, Roux M, Ryckebüsch L, Niederreither K, et al. 2011. Hox genes define distinct progenitor sub-domains within the second heart field. Dev Biol 353:266-274.
9. Bettex-Galland M, Hughes GM. 1973. Contractile filamentous material in the pillar cells of fish gills. J Cell Sci 13:359-370.
10. Bockman DE, Redmond ME, Waldo K, Davis H, et al. 1987. Effect of neural crest ablation on development of the heart and arch arteries in the chick. Am J Anat 180:332-341.
11. Brade T, Gessert S, Kühl M, Pandur P. 2007. The amphibian second heart field: Xenopus islet-1 is required for cardiovascular development. Dev Biol 311:297-310.
12. Brown CB, Feiner L, Lu MM, Li J, et al. 2001. PlexinA2 and semaphorin signaling during cardiac neural crest development. Development 128:3071-3080.
13. Calmont A, Ivins S, Van Bueren KL, Papangeli I, et al. 2009. Tbx1 controls cardiac neural crest cell migration during arch artery development by regulating Gbx2 expression in the pharyngeal ectoderm. Development 136:3173-3183.
14. Cebra-Thomas JA, Betters E, Yin M, Plafkin C, et al. 2007. Evidence that a late-emerging population of trunk neural crest cells forms the plastron bones in the turtle Trachemys scripta. Evol Dev 9:267-277.
15. Chin AJ, Saint-Jeannet J-P, Lo CW. 2012. How insights from cardiovascular developmental biology have impacted the care of infants and children with congenital heart disease. Mech Dev 129:75-97.
16. Coberly S, Lammer E, Alashari M. 1996. Retinoic acid embryopathy: case report and review of literature. Pediatr Pathol Lab Med 16:823-836.
17. De Graaf AR. 1957. Investigations into the distribution of blood in the heart and aortic arches of Xenopus laevis (Daud). J Exp Biol 34:143-172.
18. de Pater E, Clijsters L, Marques SR, Lin Y-F, et al. 2009. Distinct phases of cardiomyocyte differentiation regulate growth of the zebrafish heart. Development 136:1633-1641.
19. Delong KT. 1962. Quantitative analysis of blood circulation through the frog heart. Science 138:693-694.
20. Donoghue PCJ, Graham A, Kelsh RN. 2008. The origin and evolution of the neural crest. Bioessays 30:530-541.
21. Epperlein H-H, Selleck MAJ, Meulemans D, Mchedlishvili L, et al. 2007. Migratory patterns and developmental potential of trunk neural crest cells in the axolotl embryo. Dev Dyn 236:389-403.
22. Epperlein H-H, Meulemans D, Bronner-Fraser M, Steinbeisser H, et al. 2000. Analysis of cranial neural crest migratory pathways in axolotl using cell markers and transplantation. Development 127:2751-2761.
23. Ericsson R, Cerny R, Falck P, Olsson L. 2004. Role of cranial neural crest cells in visceral arch muscle positioning and morphogenesis in the Mexican axolotl, Ambystoma mexicanum. Dev Dyn 231:237-247.
24. Ericsson R, Joss J, Olsson L. 2008. The fate of cranial neural crest cells in the Australian lungfish, Neoceratodus forsteri. J Exp Zool Part B 310:345-354.
25. Farmer CG. 1999. Evolution of the vertebrate cardio-pulmonary system. Annu Rev Physiol 61:573-592.
26. Feiner L, Webber AL, Brown CB, Lu MM, et al. 2001. Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption. Development 128:3061-3070.
27. Frank D, Fotheringham L, Brewer J, Muglia L, et al. 2002. An Fgf8 mouse mutant phenocopies human 22q11 deletion syndrome. Development 129:4591-4603.
28. Garg V, Yamagishi C, Hu T, Kathiriya IS, et al. 2001. Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev Biol 235:62-73.
29. Gessert S, Kuehl M. 2009. Comparative gene expression analysis and fate mapping studies suggest an early segregation of cardiogenic lineages in Xenopus laevis. Dev Biol 334:395-408.
30. Geyer SH, Weninger WJ. 2012. Some mice feature 5th pharyngeal arch arteries and double-lumen aortic arch malformations. Cells Tissues Organs (Print) 196:90-98.
31. Gillis JA, Modrell MS, Baker CVH. 2013. Developmental evidence for serial homology of the vertebrate jaw and gill arch skeleton. Nat Commun 4:1436.
32. Grimes AC, Durán AC, Sans-Coma V, Hami D, et al. 2010. Phylogeny informs ontogeny: a proposed common theme in the arterial pole of the vertebrate heart. Evol Dev 12:552-567.
33. Guris DL, Duester G, Papaioannou VE, Imamoto A. 2006. Dose-dependent interaction of Tbx1 and Crkl and locally aberrant RA signaling in a model of del22q11 syndrome. Dev Cell 10:81-92.
34. Guris DL, Fantes J, Tara D, Druker BJ, et al. 2001. Mice lacking the homologue of the human 22q11.2 gene CRKL phenocopy neurocristopathies of DiGeorge syndrome. Nat Genet 27:293-298.
35. Hall BK, Gillis JA. 2013. Incremental evolution of the neural crest, neural crest cells and neural crest-derived skeletal tissues. J Anat 222:19-31.
36. Hami D, Grimes AC, Tsai H-J, Kirby ML. 2011. Zebrafish cardiac development requires a conserved secondary heart field. Development 138:2389-2398.
37. High FA, Jain R, Stoller JZ, Antonucci NB, et al. 2009. Murine Jagged1/Notch signaling in the second heart field orchestrates Fgf8 expression and tissue-tissue interactions during outflow tract development. J Clin Invest 119:1986-1996.
38. Hiruma T, Hirakow R. 1995. Formation of the pharyngeal arch arteries in the chick-embryo-observations of corrosion casts by scanning electron-microscopy. Anat Embryol 191:415-423.
39. Horigome N, Myojin M, Ueki T, Hirano S, et al. 1999. Development of cephalic neural crest cells in embryos of Lampetra japonica, with special reference to the evolution of the jaw. Dev Biol 207:287-308.
40. Hu T, Yamagishi H, Maeda J, McAnally J, et al. 2004. Tbx1 regulates fibroblast growth factors in the anterior heart field through a reinforcing autoregulatory loop involving forkhead transcription factors. Development 131:5491-5502.
41. Hutson MR, Kirby ML. 2003. Neural crest and cardiovascular development: a 20-year perspective. Birth Defects Res C 69:2-13.
42. Hutson MR, Zhang P, Stadt HA, Sato AK, et al. 2006. Cardiac arterial pole alignment is sensitive to FGF8 signaling in the pharynx. Dev Biol 295:486-497.
43. Icardo JM, Brunelli E, Perrotta I, Colvee E, et al. 2005. Ventricle and outflow tract of the African lungfish Protopterus dolloi. J Morphol 265:43-51.
44. Jandzik D, Hawkins MB, Cattell MV, Cerny R, et al. 2014. Roles for FGF in lamprey pharyngeal pouch formation and skeletogenesis highlight ancestral functions in the vertebrate head. Development 141:629-638.
45. Jerome LA, Papaioannou VE. 2001. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat Genet 27:286-291.
46. Jiang X, Choudhary B, Merki E, Chien KR, et al. 2002. Normal fate and altered function of the cardiac neural crest cell lineage in retinoic acid receptor mutant embryos. Mech Dev 117:115-122.
47. Juarez M, Reyes M, Coleman T, Rotenstein L, et al. 2013. Characterization of the trunk neural crest in the bamboo shark, Chiloscyllium punctatum. J Comp Neurol 521:3303-3320.
48. Kawasaki T, Kitsukawa T, Bekku Y, Matsuda Y, et al. 1999. A requirement for neuropilin-1 in embryonic vessel formation. Development 126:4895-4902.
49. Keyte A, Hutson MR. 2012. The neural crest in cardiac congenital anomalies. Differentiation 84:25-40.
50. Keyte AL, Smith KK. 2014. Heterochrony and developmental timing mechanisms: changing ontogenies in evolution. Semin Cell Dev Biol.
51. Kirby ML, Gale TF, Stewart DE. 1983. Neural crest cells contribute to normal aorticopulmonary septation. Science 220:1059-1061.
52. Kirby ML, Turnage KL, Hays BM. 1985. Characterization of conotruncal malformations following ablation of "cardiac" neural crest. Anat Rec 213:87-93.
53. Kochilas L, Merscher-Gomez S, Lu MM, Potluri V, et al. 2002. The role of neural crest during cardiac development in a mouse model of DiGeorge syndrome. Dev Biol 251:157-166.
54. Koestner U, Shnitsar I, Linnemannstöns K, Hufton AL, et al. 2008. Semaphorin and neuropilin expression during early morphogenesis of Xenopus laevis. Dev Dyn 237:3853-3863.
55. Kokubo N, Matsuura M, Onimaru K, Tiecke E, et al. 2010. Mechanisms of heart development in the Japanese lamprey, Lethenteron japonicum. Evol Dev 12:34-44.
56. Kolker SJ, Tajchman U, Weeks DL. 2000. Confocal imaging of early heart development in Xenopus laevis. Dev Biol 218:64-73.
57. Kuratani S, Horigome N. 2000. Developmental morphology of branchiomeric nerves in a cat shark, Scyliorhinus torazame, with special reference to rhombomeres, cephalic mesoderm, and distribution patterns of cephalic crest cells. Zool. Sci. 17:893-909.
58. Lammer EJ, Chen DT, Hoar RM, Agnish ND, et al. 1985. Retinoic acid embryopathy. N Engl J Med 313:837-841.
59. Langille RM, Hall BK. 1988. Role of the neural crest in development of the trabeculae and branchial arches in embryonic sea lamprey, Petromyzon marinus (L). Development 102:301-310.
60. Lee Y-H, Saint-Jeannet J-P. 2011. Cardiac neural crest is dispensable for outflow tract septation in Xenopus. Development 138:2025-2034.
61. Lee Y-H, Williams A, Hong C-S, You Y, et al. 2013. Early development of the thymus in Xenopus laevis. Dev Dyn 242:164-178.
62. Li P, Pashmforoush M, Sucov HM. 2010. Retinoic acid regulates differentiation of the secondary heart field and TGFbeta-mediated outflow tract septation. Dev Cell 18:480-485.
63. Li Y-X, Zdanowicz M, Young L, Kumiski D, et al. 2003. Cardiac neural crest in zebrafish embryos contributes to myocardial cell lineage and early heart function. Dev Dyn 226:540-550.
64. Liem KF, Bemis WE, Walker WFJ. 2001. Functional anatomy of the vertebrates. 3rd ed. Belmont, CA: Brooks/Cole-Thomson Learning.
65. Lin C-J, Lin C-Y, Chen C-H, Zhou B, et al. 2012. Partitioning the heart: mechanisms of cardiac septation and valve development. Development 139:3277-3299.
66. Lindsay EA. 2001. Chromosomal microdeletions: dissecting del22q11 syndrome. Nat Rev Genet 2:858-868.
67. Lorandeau CG, Hakkinen LA, Moore CS. 2011. Cardiovascular development and survival during gestation in the Ts65Dn mouse model for Down syndrome. Anat Rec (Hoboken) 294:93-101.
68. Macatee TL, Hammond BP, Arenkiel BR, Francis L, et al. 2003. Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130:6361-6374.
69. Mahadevan NR, Horton AC, Gibson-Brown JJ. 2004. Developmental expression of the amphioxus Tbx1/10 gene illuminates the evolution of vertebrate branchial arches and sclerotome. Dev. Genes Evol. 214:559-566.
70. Makki N, Capecchi MR. 2012. Cardiovascular defects in a mouse model of HOXA1 syndrome. Hum Mol Genet 21:26-31.
71. Martinsen BJ, Frasier AJ, Baker CVH, Lohr JL. 2004. Cardiac neural crest ablation alters Id2 gene expression in the developing heart. Dev Biol 272:176-190.
72. McCauley DW, Bronner-Fraser M. 2003. Neural crest contributions to the lamprey head. Development 130:2317-2327.
73. Merscher S, Funke B, Epstein JA, Heyer J, et al. 2001. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 104:619-629.
74. Meulemans D, Bronner-Fraser M. 2004. Gene-regulatory interactions in neural crest evolution and development. Dev Cell 7:291-299.
75. Mohun TJ, Leong LM, Weninger WJ, Sparrow DB. 2000. The morphology of heart development in Xenopus laevis. Dev Biol 218:74-88.
76. Mongera A, Singh AP, Levesque MP, Chen Y-Y, et al. 2013. Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells. Development 140:916-925.
77. Moon AM, Guris DL, Seo J-H, Li L, et al. 2006. Crkl deficiency disrupts Fgf8 signaling in a mouse model of 22q11 deletion syndromes. Dev Cell 10:71-80.
78. Nevis K, Obregon P, Walsh C, Guner-Ataman B, et al. 2013. Tbx1 is required for second heart field proliferation in zebrafish. Dev Dyn 242:550-559.
79. Olsson L, Falck P, Lopez K, Cobb J, et al. 2001. Cranial neural crest cells contribute to connective tissue in cranial muscles in the anuran amphibian, Bombina orientalis. Dev Biol 237:354-367.
80. Park EJ, Ogden LA, Talbot A, Evans S, et al. 2006. Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development 133:2419-2433.
81. Piotrowski T, Ahn D-G, Schilling TF, Nair S, et al. 2003. The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans. Development 130:5043-5052.
82. Piotrowski T, Nüsslein-Volhard C. 2000. The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish (Danio rerio). Dev Biol 225:339-356.
83. Reinke EE. 1910. Note on the presence of the fifth aortic arch in a 6 mm pig embryo. Anat Rec 4:453-459.
84. Roberts C, Ivins S, Cook AC, Baldini A, et al. 2006. Cyp26 genes a1, b1 and c1 are down-regulated in Tbx1 null mice and inhibition of Cyp26 enzyme function produces a phenocopy of DiGeorge syndrome in the chick. Hum Mol Genet 15:3394-3410.
85. Rochais F, Dandonneau M, Mesbah K, Jarry T, et al. 2009. Hes1 is expressed in the second heart field and is required for outflow tract development. PLoS One 4, e6267.
86. Ryckebüsch L, Wang Z, Bertrand N, Lin S-C, et al. 2008. Retinoic acid deficiency alters second heart field formation. Proc Natl Acad Sci USA 105:2913-2918.
87. Sadaghiani B, Thiébaud CH. 1987. Neural crest development in the Xenopus laevis embryo, studied by interspecific transplantation and scanning electron microscopy. Dev Biol 124:91-110.
88. Sato A, Scholl AM, Kuhn EB, Stadt HA, et al. 2011. FGF8 signaling is chemotactic for cardiac neural crest cells. Dev Biol.
89. Sato M, Tsai H-J, Yost HJ. 2006. Semaphorin3D regulates invasion of cardiac neural crest cells into the primary heart field. Dev Biol 298:12-21.
90. Sato M, Yost HJ. 2003. Cardiac neural crest contributes to cardiomyogenesis in zebrafish. Dev Biol 257:127-139.
91. Sauka-Spengler T, Le Mentec C, Lepage M, Mazan S. 2002. Embryonic expression of Tbx1, a DiGeorge syndrome candidate gene, in the lamprey Lampetra fluviatilis. Gene Expr Patterns 2:99-103.
92. Schilling TF, Kimmel CB. 1994. Segment and cell-type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120:483-494.
93. Sirbu IO, Zhao X, Duester G. 2008. Retinoic acid controls heart anteroposterior patterning by down-regulating Isl1 through the Fgf8 pathway. Dev Dyn 237:1627-1635.
94. Stolfi A, Gainous TB, Young JJ, Mori A, et al. 2010. Early chordate origins of the vertebrate second heart field. Science 329:565-568.
95. Tazumi S, Yabe S, Uchiyama H. 2010. Paraxial T-box genes, Tbx6 and Tbx1, are required for cranial chondrogenesis and myogenesis. Dev Biol 346:170-180.
96. Théveniau-Ruissy M, Dandonneau M, Mesbah K, Ghez O, et al. 2008. The del22q11.2 candidate gene Tbx1 controls regional outflow tract identity and coronary artery patterning. Circ Res 103:142-148.
97. Toyofuku T, Yoshida J, Sugimoto T, Yamamoto M, et al. 2008. Repulsive and attractive semaphorins cooperate to direct the navigation of cardiac neural crest cells. Dev Biol 321:251-262.
98. Tran HT, Delvaeye M, Verschuere V, Descamps E, et al. 2011. ARVCF depletion cooperates with Tbx1 deficiency in the development of 22q11.2DS-like phenotypes in Xenopus. Dev Dyn 240:2680-2687.
99. van den Hoff MJ, Moorman AF, Ruijter JM, Lamers WH, et al. 1999. Myocardialization of the cardiac outflow tract. Dev Biol 212:477-490.
100. Vitelli F, Morishima M, Taddei I, Lindsay EA, et al. 2002a. Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum Mol Genet 11:915-922.
101. Vitelli F, Taddei I, Morishima M, Meyers EN, et al. 2002b. A genetic link between Tbx1 and fibroblast growth factor signaling. Development 129:4605-4611.
102. Waldo K, Miyagawa-Tomita S, Kumiski D, Kirby ML. 1998. Cardiac neural crest cells provide new insight into septation of the cardiac outflow tract: aortic sac to ventricular septal closure. Dev Biol 196:129-144.
103. Waldo K, Zdanowicz M, Burch J, Kumiski DH, et al. 1999. A novel role for cardiac neural crest in heart development. J Clin Invest 103:1499-1507.
104. Waldo KL, Hutson MR, Stadt HA, Zdanowicz M, et al. 2005. Cardiac neural crest is necessary for normal addition of the myocardium to the arterial pole from the secondary heart field. Dev Biol 281:66-77.
105. Ward C, Stadt H, Hutson M, Kirby ML. 2005. Ablation of the secondary heart field leads to tetralogy of Fallot and pulmonary atresia. Dev Biol 284:72-83.
106. Xia Z, Tong X, Liang F, Zhang Y, et al. 2013. Eif3ba regulates cranial neural crest development by modulating p53 in zebrafish. Dev Biol 381:83-96.
107. Xu H, Morishima M, Wylie JN, Schwartz RJ, et al. 2004. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development 131:3217-3227.
108. Yagi H, Furutani Y, Hamada H, Sasaki T, et al. 2003. Role of TBX1 in human del22q11.2 syndrome. Lancet 362:1366-1373.
109. Yelbuz TM, Waldo KL, Kumiski DH, Stadt HA, et al. 2002. Shortened outflow tract leads to altered cardiac looping after neural crest ablation. Circulation 106:504-510.
110. Zaffran S, Kelly RG. 2012. New developments in the second heart field. Differentiation 84:17-24.
111. Zhang Z, Cerrato F, Xu H, Vitelli F, et al. 2005. Tbx1 expression in pharyngeal epithelia is necessary for pharyngeal arch artery development. Development 132:5307-5315.
112. Zhou Y, Cashman TJ, Nevis KR, Obregon P, et al. 2011. Latent TGF-β binding protein 3 identifies a second heart field in zebrafish. Nature 474:645-648.