Redundant and dosage sensitive requirements for Fgf3 and Fgf10 in cardiovascular development

Developmental Biology

Volumn 356, Issue 2, 2011, Pages 383-397

  Urness, Lisa D ^a   Bleyl, Steven B ^a   Wright, Tracy J ^a   Moon, Anne M ^a   Mansour, Suzanne L ^a  

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

Author keywords

Cardiovascular development; FGF signaling; Mouse genetics

Indexed keywords

FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 3;

ALLELE; ANIMAL TISSUE; ARTERY; ARTICLE; CARDIOVASCULAR DEVELOPMENT; CARDIOVASCULAR MALFORMATION; CARDIOVASCULAR SYSTEM; CONTROLLED STUDY; DEVELOPMENT; DISEASE SEVERITY; DORSAL MESENCHYMAL PROTRUSION; EMBRYO; EMBRYO DEATH; ENDOCARDIAL CUSHION DEFECT; EPICARDIUM; FGF10 GENE; FGF3 GENE; FOURTH PHARYNGEAL ARCH ARTERY; GENE; GENE MUTATION; GENOTYPE; HEART LEFT VENTRICLE OUTFLOW TRACT; HEART MUSCLE; HEART VENTRICLE SEPTUM DEFECT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY MALFORMATION; STEM CELL; SURVIVAL;

MURINAE;

EID: 79960561173     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.05.671     Document Type: Article

References (75)

1. Abu-Issa R., Kirby M.L. Heart field: from mesoderm to heart tube. Annu. Rev. Cell Dev. Biol. 2007, 23:45-68.
2. Abu-Issa R., Smyth G., Smoak I., Yamamura K., Meyers E.N. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 2002, 129:4613-4625.
3. Aggarwal V.S., Liao J., Bondarev A., Schimmang T., Lewandoski M., Locker J., Shanske A., Campione M., Morrow B.E. Dissection of Tbx1 and Fgf interactions in mouse models of 22q11DS suggests functional redundancy. Hum. Mol. Genet. 2006, 15:3219-3228.
4. Alvarez Y., Alonso M.T., Vendrell V., Zelarayan L.C., Chamero P., Theil T., Bösl M.R., Kato S., Maconochie M., Riethmacher D., Schimmang T. Requirements for FGF3 and FGF10 during inner ear formation. Development 2003, 130:6329-6338.
5. Azhar M., Wang P.Y., Frugier T., Koishi K., Deng C., Noakes P.G., McLennan I.S. Myocardial deletion of Smad4 using a novel alpha skeletal muscle actin Cre recombinase transgenic mouse causes misalignment of the cardiac outflow tract. Int. J. Biol. Sci. 2010, 6:546-555.
6. Bleyl S.B., Saijoh Y., Bax N.A., Gittenberger-de Groot A.C., Wisse L.J., Chapman S.C., Hunter J., Shiratori H., Hamada H., Yamada S., Shiota K., Klewer S.E., Leppert M.F., Schoenwolf G.C. Dysregulation of the PDGFRA gene causes inflow tract anomalies including TAPVR: integrating evidence from human genetics and model organisms. Hum. Mol. Genet. 2010, 19:1286-1301.
7. Brown C.B., Wenning J.M., Lu M.M., Epstein D.J., Meyers E.N., Epstein J.A. Cre-mediated excision of Fgf8 in the Tbx1 expression domain reveals a critical role for Fgf8 in cardiovascular development in the mouse. Dev. Biol. 2004, 267:190-202.
8. Bruneau B.G. The developmental genetics of congenital heart disease. Nature 2008, 451:943-948.
9. Cai C.L., Liang X., Shi Y., Chu P.H., Pfaff S.L., Chen J., Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 2003, 5:877-889.
10. Carmona R., Guadix J.A., Cano E., Ruiz-Villalba A., Portillo-Sánchez V., Pérez-Pomares J.M., Munoz-Chápuli R. The embryonic epicardium: an essential element of cardiac development. J. Cell. Mol. Med. 2010, 14:2066-2072.
11. Chien K.R., Domian I.J., Parker K.K. Cardiogenesis and the complex biology of regenerative cardiovascular medicine. Science 2008, 322:1494-1497.
12. Chisaka O., Musci T.S., Capecchi M.R. Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6. Nature 1992, 355:516-520.
13. Conway S.J., Kruzynska-Frejtag A., Kneer P.L., Machnicki M., Koushik S.V. What cardiovascular defect does my prenatal mouse mutant have, and why?. Genesis 2003, 35:1-21.
14. Dyer L.A., Kirby M.L. The role of secondary heart field in cardiac development. Dev. Biol. 2009, 336:137-144.
15. Frank D.U., Fotheringham L.K., Brewer J.A., Muglia L.J., Tristani-Firouzi M., Capecchi M.R., Moon A.M. An Fgf8 mouse mutant phenocopies human 22q11 deletion syndrome. Development 2002, 129:4591-4603.
16. Gittenberger-de Groot A.C., Winter E.M., Poelmann R.E. Epicardium-derived cells (EPDCs) in development, cardiac disease and repair of ischemia. J. Cell. Mol. Med. 2010, 14:1056-1060.
17. Goddeeris M.M., Rho S., Petiet A., Davenport C.L., Johnson G.A., Meyers E.N., Klingensmith J. Intracardiac septation requires hedgehog-dependent cellular contributions from outside the heart. Development 2008, 135:1887-1895.
18. Hatch E.P., Noyes C.A., Wang X., Wright T.J., Mansour S.L. Fgf3 is required for dorsal patterning and morphogenesis of the inner ear epithelium. Development 2007, 134:3615-3625.
19. Hoffmann A.D., Peterson M.A., Friedland-Little J.M., Anderson S.A., Moskowitz I.P. Sonic hedgehog is required in pulmonary endoderm for atrial septation. Development 2009, 136:1761-1770.
20. Ilagan R., Abu-Issa R., Brown D., Yang Y.P., Jiao K., Schwartz R.J., Klingensmith J., Meyers E.N. Fgf8 is required for anterior heart field development. Development 2006, 133:2435-2445.
21. Itoh N., Ornitz D.M. Functional evolutionary history of the mouse Fgf gene family. Dev. Dyn. 2008, 237:18-27.
22. Jia Q., McDill B.W., Li S.Z., Deng C., Chang C.P., Chen F. Smad signaling in the neural crest regulates cardiac outflow tract remodeling through cell autonomous and non-cell autonomous effects. Dev. Biol. 2007, 311:172-184.
23. Kelly R.G., Brown N.A., Buckingham M.E. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell 2001, 1:435-440.
24. Kirby M.L., Hutson M.R. Factors controlling cardiac neural crest cell migration. Cell Adh. Migr. 2010, 4. Epub ahead of print.
25. Kirby M.L., Turnage K.L., Hays B.M. Characterization of conotruncal malformations following ablation of "cardiac" neural crest. Anat. Rec. 1985, 213:87-93.
26. Ko S.O., Chung I.H., Xu X., Oka S., Zhao H., Cho E.S., Deng C., Chai Y. Smad4 is required to regulate the fate of cranial neural crest cells. Dev. Biol. 2007, 312:435-447.
27. Ladher R.K., Wright T.J., Moon A.M., Mansour S.L., Schoenwolf G.C. FGF8 initiates inner ear induction in chick and mouse. Genes Dev. 2005, 19:603-613.
28. Lie-Venema H., van den Akker N.M., Bax N.A., Winter E.M., Maas S., Kekarainen T., Hoeben R.C., deRuiter M.C., Poelmann R.E., Gittenberger-de Groot A.C. Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development. ScientificWorldJournal 2007, 7:1777-1798.
29. Lindsay E.A., Vitelli F., Su H., Morishima M., Huynh T., Pramparo T., Jurecic V., Ogunrinu G., Sutherland H.F., Scambler P.J., Bradley A., Baldini A. Tbx1 haploinsufficiency in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 2001, 410:97-101.
30. Macatee T.L., Hammond B.P., Arenkiel B.R., Francis L., Frank D.U., Moon A.M. Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 2003, 130:6361-6374.
31. Männer J., Pérez-Pomares J.M., Macías D., Muñoz-Chápuli R. The origin, formation and developmental significance of the epicardium: a review. Cells Tissues Organs 2001, 169:89-103.
32. Männer J., Schlueter J., Brand T. Experimental analyses of the function of the proepicardium using a new microsurgical procedure to induce loss-of-proepicardial-function in chick embryos. Dev. Dyn. 2005, 233:1454-1463.
33. Mansour S.L., Goddard J.M., Capecchi M.R. Mice homozygous for a targeted disruption of the proto-oncogene int-2 have developmental defects in the tail and inner ear. Development 1993, 117:13-28.
34. Marguerie A., Bajolle F., Zaffran S., Brown N.A., Dickson C., Buckingham M.E., Kelly R.G. Congenital heart defects in Fgfr2-IIIb and Fgf10 mutant mice. Cardiovasc. Res. 2006, 71:50-60.
35. McCulley D.J., Kang J.O., Martin J.F., Black B.L. 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.
36. Meyers E.N., Martin G.R. Differences in left-right axis pathways in mouse and chick: functions of FGF8 and SHH. Science 1999, 285:403-406.
37. Min H., Danilenko D.M., Scully S.A., Bolon B., Ring B.D., Tarpley J.E., DeRose M., Simonet W.S. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 1998, 12:3156-3161.
38. Mommersteeg M.T., Dominguez J.N., Wiese C., Norden J., de Gier-de Vries C., Burch J.B., Kispert A., Brown N.A., Moorman A.F., Christoffels V.M. The sinus venosus progenitors separate and diversify from the first and second heart fields early in development. Cardiovasc. Res. 2010, 87:92-101.
39. Moon A. Mouse models of congenital cardiovascular disease. Curr. Top. Dev. Biol. 2008, 84:171-248.
40. Nie X., Deng C.X., Wang Q., 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.
41. Nomura-Kitabayashi A., Phoon C.K., Kishigami S., Rosenthal J., Yamauchi Y., Abe K., Yamamura K., Samtani R., Lo C.W., Mishina Y. Outflow tract cushions perform a critical valve-like function in the early embryonic heart requiring BMPRIA-mediated signaling in cardiac neural crest. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H1617-H1628.
42. Park E.J., Ogden L.A., Talbot A., Evans S., Cai C.L., Black B.L., Frank D.U., Moon A.M. Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development 2006, 133:2419-2433.
43. Park E.J., Watanabe Y., Smyth G., Miyagawa-Tomita S., Meyers E., Klingensmith J., Camenisch T., Buckingham M., Moon A.M. An FGF autocrine loop initiated in second heart field mesoderm regulates morphogenesis at the arterial pole of the heart. Development 2008, 135:3599-3610.
44. Pérez-Pomares J.M., Phelps A., Sedmerova M., Carmona R., González-Iriarte M., Muñoz-Chápuli R., Wessels A. Experimental studies on the spatiotemporal expression of WT1 and RALDH2 in the embryonic avian heart: a model for the regulation of myocardial and valvuloseptal development by epicardially derived cells (EPDCs). Dev. Biol. 2002, 247:307-326.
45. Pérez-Pomares J.M., Phelps A., Sedmerova M., Wessels A. Epicardial-like cells on the distal arterial end of the cardiac outflow tract do not derive from the proepicardium but are derivatives of the cephalic pericardium. Dev. Dyn. 2003, 227:56-68.
46. Ponticos M. The role of the homeodomain transcription factor Nkx2-5 in the cardiovascular system. Advances in Vascular Medicine 2010, 113-130. Springer, London. D. Abraham (Ed.).
47. Qi X., Yang G., Yang L., Lan Y., Weng T., Wang J., Wu Z., Xu J., Gao X., Yang X. Essential role of Smad4 in maintaining cardiomyocyte proliferation during murine embryonic heart development. Dev. Biol. 2007, 311:136-146.
48. Ratajska A., Czarnowska E., Ciszek B. Embryonic development of the proepicardium and coronary vessels. Int. J. Dev. Biol. 2008, 52:229-236.
49. Reese D.E., Mikawa T., Bader D.M. Development of the coronary vessel system. Circ. Res. 2002, 91:761-768.
50. Rochais F., Mesbah K., Kelly R.G. Signaling pathways controlling second heart field development. Circ. Res. 2009, 104:933-942.
51. Rohmann E., Brunner H.G., Kayserili H., Uyguner O., Nürnberg G., Lew E.D., Dobbie A., Eswarakumar V.P., Uzumcu A., Ulubil-Emeroglu M., Leroy J.G., Li Y., Becker C., Lehnerdt K., Cremers C.W., Yüksel-Apak M., Nürnberg P., Kubisch C., Schlessinger J., van Bokhoven H., Wollnik B. Mutations in different components of FGF signaling in LADD syndrome. Nat. Genet. 2006, 38:414-417.
52. Sekine K., Ohuchi H., Fujiwara M., Yamasaki M., Yoshizawa T., Sato T., Yagishita N., Matsui D., Koga Y., Itoh N., Kato S. Fgf10 is essential for limb and lung formation. Nat. Genet. 1999, 21:138-141.
53. Snarr B.S., O'Neal J.L., Chintalapudi M.R., Wirrig E.E., Phelps A.L., Kubalak S.W., Wessels A. Isl1 expression at the venous pole identifies a novel role for the second heart field in cardiac development. Circ. Res. 2007, 101:971-974.
54. Snarr B.S., Wirrig E.E., Phelps A.L., Trusk T.C., Wessels A. A spatiotemporal evaluation of the contribution of the dorsal mesenchymal protrusion to cardiac development. Dev. Dyn. 2007, 236:1287-1294.
55. Snarr B.S., Kern C.B., Wessels A. Origin and fate of cardiac mesenchyme. Dev. Dyn. 2008, 237:2804-2819.
56. Snider P., Olaopa M., Firulli A.B., Conway S.J. Cardiovascular development and the colonizing cardiac neural crest lineage. ScientificWorldJournal 2007, 7:1090-1113.
57. Song L., Yan W., Chen X., Deng C.X., Wang Q., Jiao K. Myocardial Smad4 is essential for cardiogenesis in mouse embryos. Circ. Res. 2007, 101:277-285.
58. Stottmann R.W., Choi M., Mishina Y., Meyers E.N., Klingensmith J. BMP receptor IA is required in mammalian neural crest cells for development of the cardiac outflow tract and ventricular myocardium. Development 2004, 131:2205-2218.
59. Tekin M., Öztürkmen Akay H., Fitoz S., Birnbaum S., Cengiz F.B., Sennaroglu L., Incesulu A., Yüksel Konuk E.B., Hasanefendioglu Bayrak A., Sentürk S., Cebeci I., Ütine G.E., Tunçbilek E., Nance W.E., Duman D. Homozygous FGF3 mutations result in congenital deafness with inner ear agenesis, microtia, and microdontia. Clin. Genet. 2008, 73:554-565.
60. Torlopp A., Schlueter J., Brand T. Role of fibroblast growth factor signaling during proepicardium formation in the chick embryo. Dev. Dyn. 2010, 239:2393-2403.
61. Urness L.D., Paxton C.N., Wang X., Schoenwolf G.C., Mansour S.L. FGF signaling regulates otic placode induction and refinement by controlling both ectodermal target genes and hindbrain Wnt8a. Dev. Biol. 2010, 340:595-604.
62. van Wijk B., van den Berg G., Abu-Issa R., Barnett P., van der Velden S., Schmidt M., Ruijter J.M., Kirby M.L., Moorman A.F., van den Hoff M.J. Epicardium and myocardium separate from a common precursor pool by crosstalk between bone morphogenetic protein- and fibroblast growth factor-signaling pathways. Circ. Res. 2009, 105:431-441.
63. Vincent S.D., Buckingham M.E. How to make a heart: the origin and regulation of cardiac progenitor cells. Curr. Top. Dev. Biol. 2010, 90:1-41.
64. Vincentz J.W., McWhirter J.R., Murre C., Baldini A., Furuta Y. Fgf15 is required for proper morphogenesis of the mouse cardiac outflow tract. Genesis 2005, 41:192-201.
65. Virágh S., Challice C.E. The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat. Rec. 1981, 201:157-168.
66. Vitelli F., Taddei I., Morishima M., Meyers E.N., Lindsay E.A., Baldini A. A genetic link between Tbx1 and fibroblast growth factor signaling. Development 2002, 129:4605-4611.
67. Waldo K.L., Kumiski D., Kirby M.L. Cardiac neural crest is essential for the persistence rather than the formation of an arch artery. Dev. Dyn. 1996, 205:281-292.
68. Ward C., Stadt H., Hutson M., Kirby M.L. Ablation of the secondary heart field leads to tetralogy of Fallot and pulmonary atresia. Dev. Biol. 2005, 284:72-83.
69. Watanabe Y., Miyagawa-Tomita S., Vincent S.D., Kelly R.G., Moon A.M., Buckingham M.E. Role of mesodermal FGF8 and FGF10 overlaps in the development of the arterial pole of the heart and pharyngeal arch arteries. Circ. Res. 2010, 106:495-503.
70. Wright T.J., Mansour S.L. Fgf3 and Fgf10 are required for mouse otic placode induction. Development 2003, 130:3379-3390.
71. Wright T.J., Ladher R., McWhirter J., Murre C., Schoenwolf G.C., Mansour S.L. Mouse FGF15 is the ortholog of human and chick FGF19, but is not uniquely required for otic induction. Dev. Biol. 2004, 269:264-275.
72. Xu C., Liguori G., Persico M.G., Adamson E.D. Abrogation of the Cripto gene in mouse leads to failure of postgastrulation morphogenesis and lack of differentiation of cardiomyocytes. Development 1999, 126:483-494.
73. Yang L., Cai C.L., Lin L., Qyang Y., Chung C., Monteiro R.M., Mummery C.L., Fishman G.I., Cogen A., Evans S. Isl1Cre reveals a common Bmp pathway in heart and limb development. Development 2006, 133:1575-1585.
74. Zhang J., Lin Y., Zhang Y., Lan Y., Lin C., Moon A.M., Schwartz R.J., Martin J.F., Wang F. Frs2α-deficiency in cardiac progenitors disrupts a subset of FGF signals required for outflow tract morphogenesis. Development 2008, 135:3611-3622.
75. Zhou W., Lin L., Majumdar A., Li X., Zhang X., Liu W., Etheridge L., Shi Y., Martin J., Van de Ven W., Kaartinen V., Wynshaw-Boris A., McMahon A.P., Rosenfeld M.G., Evans S.M. Modulation of morphogenesis by noncanonical Wnt signaling requires ATF/CREB family-mediated transcriptional activation of TGFbeta2. Nat. Genet. 2007, 39:1225-1234.