Myocardial deletion of Smad4 using a novel α skeletal muscle actin cre recombinase transgenic mouse causes misalignment of the cardiac outflow tract

International Journal of Biological Sciences

Volumn 6, Issue 6, 2010, Pages 546-555

  Azhar, Mohamad ^a   Wang, Pei Yu ^b,c   Frugier, Tony ^b,d   Koishi, Kyoko ^b   Deng, Chuxia ^e   Noakes, Peter G ^f   Mclennan, Ian S ^b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c NATIONAL CHENGCHI UNIVERSITY   (Taiwan)

^d NATIONAL TRAUMA RESEARCH INSTITUTE   (Australia)

^e NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^f UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Heart; Marfan syndrome; Myogenesis; SMAD; Transforming growth factor beta

Indexed keywords

MUS; MUS MUSCULUS;

EID: 78650047563     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijbs.6.546     Document Type: Article

References (55)

1. Pierpont ME, Basson CT, Benson DW Jr, et al. Genetic basis for congenital heart defects current knowledge a scientific statement from the American Heart Association Congenital Cardiac Defects Committee Council on Cardiovascular Disease in the Young endorsed by the American Academy of Pediatrics. Circulation. 2007; 115:3015-3038.
2. Markwald RR, Norris RA, Moreno-Rodriguez R, and Levine RA. Developmental basis of adult cardiovascular diseases valvular heart diseases. Ann N Y Acad Sci. 2010; 1188:177-83.
3. Gittenberger-de Groot AC, Bartelings MM, DeRuiter MC and Poelmann RE. Basics of cardiac development for the understanding of congenital heart malformations. Pediatr Res. 2005; 57:169-176.
4. Person AD, Klewer SE, and Runyan RB. Cell biology of cardiac cushion development. Int Rev Cytol. 2005; 243:287-335.
5. Barnett JV and Desgrosellier JS. Earl y events i n val vul ogenesi s a signaling perspective. Birth Defects Res C Embryo Today. 2003; 69:58-72.
6. Combs MD and Yutzey KE. Heart valve development regulatory networks in development and disease. Circ Res. 2009; 105:408-421.
7. Azhar M, Schultz JE, Grupp I, et al. Transforming growth factor beta in cardiovascular development and function. Cytokine Growth Factor Rev. 2003; 14:391-407.
8. Delot EC. Control of endocardial cushion and cardiac valve maturation by BMP signaling pathways. Mol Genet Metab 2003; 80:27-35.
9. Molin DG, Bartram U, Van der HK, et al. Expression patterns of Tgfbeta1-3 associate with myocardialisation of the outflow tract and the development of the epicardium and the fibrous heart skeleton. Dev Dyn. 2003; 227:431-444.
10. Azhar M, Runyan RB, Gard C, et al. Ligand-specific function of transforming growth factor beta in epithelial-mesenchymal transition in heart development. Dev Dyn. 2009; 238:431-442.
11. Compton LA, Potash DA, Brown CB, and Barnett JV. Coronary vessel development is dependent on the type III transforming growth factor beta receptor. Circ Res. 2007; 101:784-791.
12. Bartram U, Molin DG, Wisse LJ, et al. Double-outlet right ventricle and overriding tricuspid valve reflect disturbances of looping myocardialization endocardial cushion differentiation and apoptosis in Tgfb2 knockout mice. Circulation. 2001; 103:2745-2752.
13. Uchimura T, Komatsu Y, Tanaka M, et al. Bmp2 and Bmp4 genetically interact to support multiple aspects of mouse development including functional heart development. Genesis. 2009; 47:374-384.
14. Beppu H, Malhotra R, Beppu Y, et al. BMP type II receptor regulates positioning of outflow tract and remodeling of atrioventricular cushion during cardiogenesis. Dev Biol. 2009; 331:167-175.
15. Choudhary B, Ito Y, Makita T, et al. Cardiovascular malformations with normal smooth muscle differentiation in neural crest-specific type II TGFbeta receptor (Tgfbr2) mutant mice. Dev Biol. 2006; 289:420-429.
16. Sridurongrit S, Larsson J, Schwartz R, et al. Signaling via the Tgf-beta type I receptor Alk5 in heart development. Dev Biol. 2008; 322:208-218.
17. Wang J, Sridurongrit S, Dudas M, et al. Atrioventricular cushion transformation is mediated by ALK2 in the developing mouse heart. Dev Biol. 2005; 286:299-310.
18. Ma L, Lu MF, Schwartz RJ, and Martin JF. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development. 2005; 132:5601-5611.
19. Jiao K, Langworthy M, Batts L, et al. Tgfbeta signaling is required for atrioventricular cushion mesenchyme remodeling during in vivo cardiac development. Development. 2006; 133:4585-4593.
20. Jiao K, Kulessa H, Tompkins K, et al. An essential role of Bmp4 in the atrioventricular septation of the mouse heart. Genes Dev. 2003; 17:2362-2367.
21. Camenisch TD, Molin DG, Person A, et al. Temporal and Distinct TGFbeta Ligand Requirements during Mouse and Avian Endocardial Cushion Morphogenesis. Dev Biol. 2002; 248:170-181.
22. Sugi Y, Yamamura H, Okagawa H and Markwald RR. Bone morphogenetic protein-2 can mediate myocardial regulation of atrioventricular cushion mesenchymal cell formation in mice. Dev Biol. 2004; 269:505-518.
23. Shi Y and Massague J. Mechani sms of TGF-beta signaling from cell membrane to the nucleus. Cell. 2003; 113:685-700.
24. Wharton K and Derynck R. TGFbeta family signaling novel insights in development and disease. Development. 2009; 136:3691-3697.
25. Tang S, Snider P, Firulli AB and Conway SJ. Trigenic neural crest-restricted Smad7 over-expression results in congenital craniofacial and cardiovascular defects. Dev Biol. 2010; 344:233-247.
26. Euler-Taimor G and Heger J. The complex pattern of SMAD signaling in the cardiovascular system. Cardiovasc Res. 2006; 69:15-25.
27. Galvin KM, Donovan MJ, Lynch CA, et al. A role for smad6 in development and homeostasis of the cardiovascular system. Nat Genet. 2000; 24:171-174.
28. Wang J, Xu N, Feng X, et al. Tar get ed Di sr upti on of Smad4 i n Cardiomyocytes Results in Cardiac Hypertrophy and Heart Failure. Circ Res. 2005; 97:821-828.
29. Song L, Yan W, Chen X, et al. Myocardial smad4 is essential for cardiogenesis in mouse embryos. Circ Res. 2007; 101:277-285.
30. Qi X, Yang G, Yang L, et al. Essential role of Smad4 in maintaining cardiomyocyte proliferation during murine embryonic heart development. Dev Biol. 2007; 311:136-146.
31. Sirard C, de la Pompa JL, Elia A, et al. The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev. 1998; 12:107-119.
32. Wang RH, Li C, Xu X, et al. A role of SMAD4 in iron metabolism through the positive regulation of hepcidin expression. Cell Metab. 2005; 2:399-409.
33. Xu X, Ehdaie B, Ohara N, et al. Synergistic action of Smad4 and Pten in suppressing pancreatic ductal adenocarcinoma formation in mice. Oncogene. 2010; 29:674-686.
34. Yang G and Yang X. Smad4-mediated TGF-beta signaling in tumorigenesis. Int J Biol Sci. 2010; 6:1-8.
35. McLennan IS and Taylor-Jeffs J. The use of sodium lamps to brightly illuminate mouse houses during their dark phases. Lab Anim. 2004; 38:1-9.
36. Yang X, Li C, Herrera PL, and Deng CX. Generation of Smad4/Dpc4 conditional knockout mice. Genesis. 2002; 32:80-81.
37. Friedrich G and Soriano P. Promoter traps in embryonic stem cells a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 1991; 5:1513-1523.
38. Brennan KJ and Hardeman EC. Quantitative analysis of the human alpha-skeletal actin gene in transgenic mice. J Biol Chem. 1993; 268:719-725.
39. Feil R, Brocard J, Mascrez B, et al. Ligand-activated site-specific recombination in mice. Proc Natl Acad Sci USA. 1996; 93:10887-10890.
40. Frugier T, Koishi K, Matthaei KI and McLennan IS. Transgenic mice carrying a tetracycline-inducible truncated transforming growth factor beta receptor (TbetaRII). Genesis. 2005; 42:1-5.
41. Lobe CG, Koop KE, Kreppner W, et al. Z/AP a double reporter for cre-mediated recombination. Dev Biol. 1999; 208:281-292.
42. Wang PY, Protheroe A, Clarkson AN, et al. Mullerian inhibiting substance contributes to sex-linked biases in the brain and behavior. Proc Natl Acad Sci USA. 2009; 106:7203-7208.
43. Sohal DS, Nghiem M, Crackower MA, et al. Temporally regulated and tissue-specific gene manipulations in the adult and embryonic heart using a tamoxifen-inducible Cre protein. Circ Res. 2001; 89:20-25.
44. Grieshammer U, Lewandoski M, Prevette D, et al. (1998) Muscle-specific cell ablation conditional upon Cre-mediated DNA recombination in transgenic mice leads to massive spinal and cranial motoneuron loss. Dev Biol. 1998; 197:234-247.
45. Li P, Pashmforoush M and Sucov HM. Retinoic acid regulates differentiation of the secondary heart field and TGFbeta- mediated outflow tract septation. Dev Cell. 2010; 18:480-485.
46. McCull ey DJ, Kang JO, Marti n JF and Bl ack BL. (2008) BMP4 is required in the anterior heart field and its derivatives for endocardial cushion remodeling outflow tract septation and semilunar valve development. Dev Dyn. 2008; 237:3200-3209.
47. Lan Y, Liu B, Yao H, et al. Essential role of endothelial Smad4 in vascular remodeling and integrity. Mol Cell Biol. 2007; 27:7683-7692.
48. Nie X, Deng CX, Wang Q and Jiao K. Disruption of Smad4 in neural crest cells leads to mid-gestation death with pharyngeal arch craniofacial and cardiac defects. Dev Biol. 2008; 316:417-430.
49. Kallapur S, Ormsby I, and Doetschman T. Strain dependency of TGFbeta1 function during embryogenesis. Mol Reprod Dev. 1999; 52:341-349.
50. Tang Y, Lee KS, Yang H, et al. Epistatic interactions between modifier genes confer strain-specific redundancy for Tgfb1 in developmental angiogenesis. Genomics. 2005; 85:60-70.
51. Asano Y, Koishi K, Frugier T and McLennan IS. Mice with disrupted TGFbeta signaling have normal cerebella development but exhibit facial dysmorphogenesis and strain-dependent deficits in their body wall. Cell Mol Neurobiol. 2009; 29:621-633.
52. Engle SJ, Ormsby I, Pawlowski S, et al. Elimination of colon cancer in germ-free Transforming Growth Factor beta 1-deficient mice. Cancer Res. 2002; 62:6362-6366.
53. Sanford LP, Ormsby I, Gittenberger-de GA, et al. TGFbeta2 knockout mice have multiple developmental defects that are non- overlapping with other TGFbeta knockout phenotypes. Development 1997; 124:2659-2670.
54. Xu J, Ismat FA, Wang T, et al. Cardiomyocyte-specific loss of neurofibromin promotes cardiac hypertrophy and dysfunction. Circ Res. 2009; 105:304-311.
55. Gaussin V, Van de PT, Mishina Y, et al. Endocardial cushion and myocardial defects after cardiac myocyte-specific conditional deletion of the bone morphogenetic protein receptor ALK3. Proc Natl Acad Sci USA. 2002; 99:2878-2883.