Muscle connective tissue controls development of the diaphragm and is a source of congenital diaphragmatic hernias

Nature Genetics

Volumn 47, Issue 5, 2015, Pages 496-504

  Merrell, Allyson J ^a   Ellis, Benjamin J ^b,c   Fox, Zachary D ^a   Lawson, Jennifer A ^a   Weiss, Jeffrey A ^b,c   Kardon, Gabrielle ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b University of Utah   (United States)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR GATA 4; GATA4 PROTEIN, MOUSE; HGF PROTEIN, MOUSE; SCATTER FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOMECHANICS; CELL MIGRATION; CONGENITAL DIAPHRAGM HERNIA; CONNECTIVE TISSUE; CONTROLLED STUDY; DIAPHRAGM MUSCLE; EMBRYONIC STRUCTURES; FIBROBLAST; GENE EXPRESSION; GENE MUTATION; MORPHOGENESIS; MOSAICISM; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; DIAPHRAGM; DISEASE MODEL; EMBRYOLOGY; GENE DELETION; GENETICS; LUNG; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; MYOBLAST; PATHOLOGY; PHYSIOLOGY; RADIOGRAPHY; TRANSGENIC MOUSE;

MAMMALIA;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; CONNECTIVE TISSUE; DIAPHRAGM; DISEASE MODELS, ANIMAL; FIBROBLASTS; GATA4 TRANSCRIPTION FACTOR; GENE DELETION; HEPATOCYTE GROWTH FACTOR; HERNIAS, DIAPHRAGMATIC, CONGENITAL; LUNG; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE DEVELOPMENT; MYOBLASTS; X-RAY MICROTOMOGRAPHY;

EID: 84929132091     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3250     Document Type: Article

References (62)

1. Perry, S.F., Similowski, T., Klein, W. & Codd, J.R. The evolutionary origin of the mammalian diaphragm. Respir. Physiol. Neurobiol. 171, 1-16 (2010
2. Campbell, E.J.M., Agostoni, E & Newsom Davis, J. The Respiratory Muscles: Mechanics and Neural Control (Lloyd-Luke, 1970
3. Merrell, A.J. & Kardon, G. Development of the diaphragm-A skeletal muscle essential for mammalian respiration. FEBS J. 280, 4026-4035 (2013
4. Raval, M.V., Wang, X., Reynolds, M. & Fischer, A.C. Costs of congenital diaphragmatic hernia repair in the United States-extracorporeal membrane oxygenation foots the bill. J. Pediatr. Surg. 46, 617-624 (2011
5. Torfs, C.P., Curry, C.J., Bateson, T.F. & Honore, L.H. A population-based study of congenital diaphragmatic hernia. Teratology 46, 555-565 (1992
6. Pober, B.R. Overview of epidemiology, genetics, birth defects, and chromosome abnormalities associated with CDH. Am. J. Med. Genet. C. Semin. Med. Genet. 145C, 158-171 (2007
7. Pober, B.R. et al. Infants with Bochdalek diaphragmatic hernia: sibling precurrence and monozygotic twin discordance in a hospital-based malformation surveillance program. Am. J. Med. Genet. A. 138A, 81-88 (2005
8. Holder, A.M. et al. Genetic factors in congenital diaphragmatic hernia. Am. J. Hum. Genet. 80, 825-845 (2007
9. Veenma, D.C., De Klein, A. & Tibboel, D. Developmental and genetic aspects of congenital diaphragmatic hernia. Pediatr. Pulmonol. 47, 534-545 (2012
10. Russell, M.K. et al. Congenital diaphragmatic hernia candidate genes derived from embryonic transcriptomes. Proc. Natl. Acad. Sci. USA 109, 2978-2983 (2012
11. Arrington, C.B. et al. A family-based paradigm to identify candidate chromosomal regions for isolated congenital diaphragmatic hernia. Am. J. Med. Genet. A. 158A, 3137-3147 (2012
12. Longoni, M. et al. Congenital diaphragmatic hernia interval on chromosome 8p23.1 characterized by genetics and protein interaction networks. Am. J. Med. Genet. A. 158A, 3148-3158 (2012
13. Yu, L. et al. Variants in GATA4 are a rare cause of familial and sporadic congenital diaphragmatic hernia. Hum. Genet. 132, 285-292 (2013
14. Kuo, C.T. et al. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 11, 1048-1060 (1997
15. Molkentin, J.D., Lin, Q., Duncan, S.A. & Olson, E.N. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11, 1061-1072 (1997
16. Jay, P.Y. et al. Impaired mesenchymal cell function in Gata4 mutant mice leads to diaphragmatic hernias and primary lung defects. Dev. Biol. 301, 602-614 (2007
17. Mendelsohn, C. et al. Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120, 2749-2771 (1994
18. You, L.R. et al. Mouse lacking COUP-TFII as an animal model of Bochdalek-type congenital diaphragmatic hernia. Proc. Natl. Acad. Sci. USA 102, 16351-16356 (2005
19. Ackerman, K.G. et al. Fog2 is required for normal diaphragm and lung development in mice and humans. PLoS Genet. 1, 58-65 (2005
20. Coles, G.L. & Ackerman, K.G. Kif7 is required for the patterning and differentiation of the diaphragm in a model of syndromic congenital diaphragmatic hernia. Proc. Natl. Acad. Sci. USA 110, E1898-E1905 (2013
21. Allan, D.W. & Greer, J.J. Embryogenesis of the phrenic nerve and diaphragm in the fetal rat. J. Comp. Neurol. 382, 459-468 (1997
22. Babiuk, R.P., Zhang, W., Clugston, R., Allan, D.W. & Greer, J.J. Embryological origins and development of the rat diaphragm. J. Comp. Neurol. 455, 477-487 (2003
23. Dietrich, S. et al. The role of SF/HGF and c-Met in the development of skeletal muscle. Development 126, 1621-1629 (1999
24. Greer, J.J. et al. Structure of the primordial diaphragm and defects associated with nitrofen-induced CDH. J. Appl. Physiol. 89, 2123-2129 (2000
25. Ackerman, K.G. & Greer, J.J. Development of the diaphragm and genetic mouse models of diaphragmatic defects. Am. J. Med. Genet. C. Semin. Med. Genet. 145C, 109-116 (2007
26. Logan, M. et al. Expression of Cre recombinase in the developing mouse limb bud driven by a Prx1 enhancer. Genesis 33, 77-80 (2002
27. Soriano, P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71 (1999
28. Kardon, G., Harfe, B.D. & Tabin, C.J.A. Tcf4-positive mesodermal population provides a prepattern for vertebrate limb muscle patterning. Dev. Cell 5, 937-944 (2003
29. Mathew, S.J. et al. Connective tissue fibroblasts and Tcf4 regulate myogenesis. Development 138, 371-384 (2011
30. Clugston, R.D., Zhang, W. & Greer, J.J. Gene expression in the developing diaphragm: significance for congenital diaphragmatic hernia. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L665-L675 (2008
31. Engleka, K.A. et al. Insertion of Cre into the Pax3 locus creates a new allele of Splotch and identifies unexpected Pax3 derivatives. Dev. Biol. 280, 396-406 (2005
32. Vogan, K.J., Epstein, D.J., Trasler, D.G. & Gros, P. The splotch-delayed (Spd) mouse mutant carries a point mutation within the paired box of the Pax-3 gene. Genomics 17, 364-369 (1993
33. Watt, A.J., Battle, M.A., Li, J. & Duncan, S.A. GATA4 is essential for formation of the proepicardium and regulates cardiogenesis. Proc. Natl. Acad. Sci. USA 101, 12573-12578 (2004
34. Ackerman, K.G. et al. Congenital diaphragmatic defects: proposal for a new classification based on observations in 234 patients. Pediatr. Dev. Pathol. 15, 265-274 (2012
35. Clugston, R.D. & Greer, J.J. Diaphragm development and congenital diaphragmatic hernia. Semin. Pediatr. Surg. 16, 94-100 (2007
36. Maas, S.A., Ellis, B.J., Ateshian, G.A. & Weiss, J.A. FEBio: finite elements for biomechanics. J. Biomech. Eng. 134, 011005 (2012
37. Strumpf, R.K., Humphrey, J.D. & Yin, F.C. Biaxial mechanical properties of passive and tetanized canine diaphragm. Am. J. Physiol. 265, H469-H475 (1993
38. Keijzer, R., Liu, J., Deimling, J., Tibboel, D. & Post, M. Dual-hit hypothesis explains pulmonary hypoplasia in the nitrofen model of congenital diaphragmatic hernia. Am. J. Pathol. 156, 1299-1306 (2000
39. Ackerman, K.G. et al. Gata4 is necessary for normal pulmonary lobar development. Am. J. Respir. Cell Mol. Biol. 36, 391-397 (2007
40. Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A. & Birchmeier, C. Essential role for the c-Met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376, 768-771 (1995
41. Maina, F. et al. Uncoupling of Grb2 from the Met receptor in vivo reveals complex roles in muscle development. Cell 87, 531-542 (1996
42. Nakamura, K., Hongo, A., Kodama, J. & Hiramatsu, Y. The role of hepatocyte growth factor activator inhibitor (HAI)-1 and HAI-2 in endometrial cancer. Int. J. Cancer 128, 2613-2624 (2011
43. Rojas, A. et al. GATA4 is a direct transcriptional activator of cyclin D2 and Cdk4 and is required for cardiomyocyte proliferation in anterior heart field-derived myocardium. Mol. Cell. Biol. 28, 5420-5431 (2008
44. Yamak, A. et al. Cyclin D2 rescues size and function of GATA4 haplo-insufficient hearts. Am. J. Physiol. Heart Circ. Physiol. 303, H1057-H1066 (2012
45. Domyan, E.T. et al. Roundabout receptors are critical for foregut separation from the body wall. Dev. Cell 24, 52-63 (2013
46. Zhang, B. et al. Heparan sulfate deficiency disrupts developmental angiogenesis and causes congenital diaphragmatic hernia. J. Clin. Invest. 124, 209-221 (2014
47. Veenma, D. et al. Copy number detection in discordant monozygotic twins of congenital diaphragmatic hernia (CDH) and esophageal atresia (EA) cohorts. Eur. J. Hum. Genet. 20, 298-304 (2012
48. Wat, M.J. et al. Chromosome 8p23.1 deletions as a cause of complex congenital heart defects and diaphragmatic hernia. Am. J. Med. Genet. A. 149A, 1661-1677 (2009
49. Kantarci, S. et al. Characterization of the chromosome 1q41q42.12 region, and the candidate gene DISP1, in patients with CDH. Am. J. Med. Genet. A. 152A, 2493-2504 (2010
50. Veenma, D. et al. Comparable low-level mosaicism in affected and non affected tissue of a complex CDH patient. PLoS ONE 5, e15348 (2010
51. Pu, W.T., Ishiwata, T., Juraszek, A.L., Ma, Q. & Izumo, S. GATA4 is a dosage-sensitive regulator of cardiac morphogenesis. Dev. Biol. 275, 235-244 (2004
52. Wat, M.J. et al. Mouse model reveals the role of SOX7 in the development of congenital diaphragmatic hernia associated with recurrent deletions of 8p23.1. Hum. Mol. Genet. 21, 4115-4125 (2012
53. Bosch, N. et al. Nucleotide, cytogenetic and expression impact of the human chromosome 8p23.1 inversion polymorphism. PLoS ONE 4, e8269 (2009
54. Giglio, S. et al. Olfactory receptor-gene clusters, genomic-inversion polymorphisms, and common chromosome rearrangements. Am. J. Hum. Genet. 68, 874-883 (2001
55. Reamon-Buettner, S.M. & Borlak, J. GATA4 zinc finger mutations as a molecular rationale for septation defects of the human heart. J. Med. Genet. 42, e32 (2005
56. Reamon-Buettner, S.M., Cho, S.H. & Borlak, J. Mutations in the 3'-untranslated region of GATA4 as molecular hotspots for congenital heart disease (CHD). BMC Med. Genet. 8, 38 (2007
57. Biesecker, L.G. & Spinner, N.B. A genomic view of mosaicism and human disease. Nat. Rev. Genet. 14, 307-320 (2013
58. Tang, S.H., Silva, F.J., Tsark, W.M. & Mann, J.R.A. Cre/loxP-deleter transgenic line in mouse strain 129S1/SvImJ. Genesis 32, 199-202 (2002
59. Muzumdar, M.D., Tasic, B., Miyamichi, K., Li, L. & Luo, L. A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605 (2007
60. Wan, Y., Otsuna, H., Chien, C.B. & Hansen, C. An interactive visualization tool for multi-channel confocal microscopy data in neurobiology research. IEEE Trans. Vis. Comput. Graph. 15, 1489-1496 (2009
61. Veronda, D.R. & Westmann, R.A. Mechanical characterization of skin-finite deformations. J. Biomech. 3, 111-124 (1970
62. Mooney, M. A theory of large elastic deformation. J. Appl. Phys. 11, 582-592 (1940