Intracardiac septation requires hedgehog-dependent cellular contributions from outside the heart

Development

Volumn 135, Issue 10, 2008, Pages 1887-1895

  Goddeeris, Matthew M ^a,b   Rho, Silvia ^a   Petiet, Alexandra ^a   Davenport, Chandra L ^a   Johnson, G Allan ^a   Meyers, Erik N ^a,c   Klingensmith, John ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c St Luke's Children's Hospital   (United States)

Author keywords

Atrioventricular septal defect; Heart development; Intracardiac septation; Morphogenesis; Mouse; Sonic hedgehog

Indexed keywords

SONIC HEDGEHOG PROTEIN; SHH PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; HEART ATRIUM SEPTUM DEFECT; HEART DEVELOPMENT; HEART VENTRICLE SEPTUM DEFECT; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MOUSE; MUTANT; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TISSUE CULTURE; ANIMAL; CYTOLOGY; FETUS HEART; GENETICS; HEART ATRIUM; HEART SEPTUM DEFECT; MESODERM; METABOLISM; MOUSE MUTANT; MUTATION; PRENATAL DEVELOPMENT;

ERINACEIDAE; MAMMALIA;

ANIMALS; FETAL HEART; HEART ATRIA; HEART SEPTAL DEFECTS, VENTRICULAR; HEDGEHOG PROTEINS; MESODERM; MICE; MICE, MUTANT STRAINS; MUTATION; SIGNAL TRANSDUCTION;

EID: 49949115945     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.016147     Document Type: Article

References (38)

1. Abu-Issa, R., Smyth, G., Smoak, I., Yamamura, K. and Meyers, E. N. (2002). Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 129, 4613-4625.
2. Bader, D., Masaki, T. and Fischman, D. A. (11982). Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol. 95, 763-770.
3. Blom, N. A., Ottenkamp, J., Wenink, A. G. and Gittenberger-de Groot, A. C. (2003). Deficiency of the vestibular spine in atrioventricular septal defects in human fetuses with down syndrome. Am. J. Cardiol. 91, 180-184.
4. Cai, C. L., Liang, X., Shi, Y., Chu, P. H., Pfaff, S. L., Chen, J. and Evans, S. (2003). Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 5, 877-889.
5. Chen, J. K., Taipale, J., Young, K. E., Maiti, T. and Beachy, P. A. (2002). Small molecule modulation of Smoothened activity. Proc. Natl. Acad. Sci. USA 99, 14071-14076.
6. de Lange, F. J., Moorman, A. F., Anderson, R. H., Manner, J., Soufan, A. T., de Gier-de Vries, C., Schneider, M. D., Webb, S., van den Hoff, M. J. and Christoffels, V. M. (2004). Lineage and morphogenetic analysis of the cardiac valves. Circ. Res. 95, 645-654.
7. Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A. and McMahon, A. P. (1993). Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430.
8. Goddeeris, M. M., Schwartz, R., Klingensmith, J. and Meyers, E. N. (2007). Independent requirements for Hedgehog signaling by both the anterior heart field and neural crest cells for outflow tract development. Development 134, 1593-1604.
9. Harfe, B. D., Scherz, P. J., Nissim, S., Tian, H., McMahon, A. P. and Tabin, C. J. (2004). Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118, 517-528.
10. His, W. (1880). Die area interposita, die Eustachische klappe und die spina vestibuli. Anatomie Menschlicher Embryonen 1880, 149-152.
11. Hoffman, J. I. (1995). Incidence of congenital heart disease. II. Prenatal incidence. Pediatr. Cardiol. 16, 155-165.
12. Hoffman, J. I. and Kaplan, S. (2002). The incidence of congenital heart disease. J. Am. Coll. Cardiol. 39, 1890-1900.
13. Hogan, B., Beddington, R., Constantini, F. and Lacy, E. (1994). Manipulating the Mouse Embryo: A Laboratory Manual. Plainview, NY: Cold Spring Harbor Laboratory Press.
14. Huynh, T., Chen, L., Terrell, P. and Baldini, A. (2007). A fate map of Tbx1 expressing cells reveals heterogeneity in the second cardiac field. Genesis 45, 470-475.
15. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
16. Jiao, K., Kulessa, H., Tompkins, K., Zhou, Y., Batts, L., Baldwin, H. S. and Hogan, B. L. (2003). An essential role of Bmp4 in the atrioventricular septation of the mouse heart. Genes Dev. 17, 2362-2367.
17. Johnson, G. A., Ali-Sharief, A., Badea, A., Brandenburg, J., Cofer, G., Fubara, B., Gewalt, S., Hedlund, L. W. and Upchurch, L. (2007). High-throughput morphologic phenotyping of the mouse brain with magnetic resonance histology. Neuroimage 37, 82-89.
18. Kelly, R. G., Brown, N. A. and Buckingham, M. E. (2001). The arterial pole of the mouse heart forms f rom Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell 1, 435-440.
19. Koni, P. A., Joshi, S. K., Temann, U.-A., Olson, D., Burkly, L. and Flavell, R. A. (2001). Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J. Exp. Med. 193, 741-754.
20. Lamers, W. H. and Moorman, A. F. (2002), Cardiac septation: a late contribution of the embryonic primary myocardium to heart morphogenesis. Circ. Res. 91, 93-103.
21. Meyers, E. N., Lewandoski, M. and Martin, G. R. (1998). An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 18, 136-141.
22. Mjaatvedt, C. H., Nakaoka, T., Moreno-Rodriguez, R., Norris, R. A., Kern, M. J., Eisenberg, C. A., Turner, D. and Markwald, R. R. (2001). The outflow tract of the heart is recruited from a novel heart-forming field. Dev. Biol. 238, 97-109.
23. Mommersteeg, M. T., Soufan, A. T., de Lange, F. J., van den Hoff, M. J., Anderson, It. H., Christoffels, V. M. and Moorman, A. F. (2006). Two distinct pools of mesenchyme contribute to the development of the atrial septum. Circ. Res. 99, 351-353.
24. Neubuser, A., Peters, H., Balling, R. and Martin, G. R. (1997). Antagonistic interactions between FGF and BMP signaling pathways: a mechanism for positioning the sites of tooth formation. Cell 90, 247-255.
25. Petiet, A., Hedlund, L. and Johnson, G. A. (2007). Staining methods for magnetic resonance microscopy of the rat fetus. J. Magn. Reson. Imaging 25, 1192-1198.
26. Snarr, B. S., Wirrig, E. E., Phelps, A. L., Trusk, T. C. and Wessels, A. (2007a). A spatiotemporal evaluation of the contribution of the dorsal mesenchymal protrusion to cardiac development. Dev. Dyn. 236, 1287-1294.
27. Snarr, B. S., O'Neal, J. L., Chintalapudi, M. R., Wirrig, E. E., Phelps, A. L., Kubalak, S. W. and Wessels, A. (2007b). Isl 1 expression at the venous pole identifies a novel role for the second heart field in cardiac development. Circ. Res. 101, 971-974.
28. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
29. Soufan, A. T., van den Hoff, M. J., Ruijter, J. M., de Boer, P. A., Hagoort, J., Webb, S., Anderson, R. H. and Moorman, A. F. (2004). Reconstruction of the patterns of gene expression in the developing mouse heart reveals an architectural arrangement that facilitates the understanding of atrial malformations and arrhythmias. Circ. Res. 95, 1207-1215.
30. Verzi, M. P., McCulley, D. J., De Val, S., Doclou, E. and Black, B. L. (2005). The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev. Biol. 287, 134-145.
31. Waldo, K. L., Kumiski, D. H., Wallis, K. T., Stadt, H. A., Hutson, M. R., Platt, D. H. and Kirby, M. L. (2001). Conotruncal myocardium arises from a secondary heart field. Development 128, 3179-3188.
32. Washington Smoak, I., Byrd, N. A., Abu-Issa, R., Goddeeris, M. M., Anderson, R., Morris, J., Yamamura, K., Klingensmith, J. and Meyers, E. N. (2005), Sonic hedgehog is required for cardiac outflow tract and neural crest cell development. Dev. Biol. 283, 357-372.
33. Webb, S., Brown, N. A. and Anderson, R. H. (1998). Formation of the atrioventricular septal structures in the normal mouse. Circ. Res. 82, 645-656.
34. Webb, S., Anderson, R. H., Lamers, W. H. and Brown, N. A. (1999). Mechanisms of deficient cardiac septation in the mouse with trisomy 16. Circ. Res. 84, 897-905.
35. Wessels, A., Anderson, R. H., Markwald, R. R., Webb, S., Brown, N. A., Viragh, S., Moorman, A. F. and Lamers, W. H. (2000). Atrial development in the human heart: an immunohistochemical study with emphasis on the role of mesenchymal tissues. Anat. Rec. 259, 288-300.
36. Wirrig, E. E., Snarr, B. S., Chintalapudi, M. R., O'Neal J. L., Phelps, A. L., Barth, J. L., Fresco, V. M., Kern, C. B., Mjaatvedt, C. H., Toole, B. P. et al. (2007). Cartilage link protein 1 (Crtl1), an extracellular matrix component playing an important role in heart development. Dev. Biol. 310, 291-303.
37. Zhang, X. M., Ramalho-Santos, M. and McMahon, A. P. (2001). Smoothened mutants reveal redundant roles for Shh and lhh signaling including regulation of L/R symmetry by the mouse node. Cell 106, 781-792.
38. Zucker, R. M., Hunter, E. S., 3rd and Rogers, J. M. (1999). Apoptosis and morphology in mouse embryos by confocal laser scanning microscopy. Methods 18, 473-480.