Fibronectin signals through integrin α5β1 to regulate cardiovascular development in a cell type-specific manner

Developmental Biology

Volumn 407, Issue 2, 2015, Pages 195-210

  Chen, Dongying ^a   Wang, Xia ^a   Liang, Dong ^a,d   Gordon, Julie ^b   Mittal, Ashok ^a,e   Manley, Nancy ^b   Degenhardt, Karl ^c   Astrof, Sophie ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b University of Georgia   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d WOMEN S HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Cardiovascular development; Fibronectin; Integrin 5; Pharyngeal arch arteries

Indexed keywords

FIBRONECTIN; VERY LATE ACTIVATION ANTIGEN 5; INSULIN GENE ENHANCER BINDING PROTEIN ISL-1; LIM HOMEODOMAIN PROTEIN; T BOX TRANSCRIPTION FACTOR; TBX1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ARTICLE; CELLS BY BODY ANATOMY; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM; GENE DELETION; HEART DEVELOPMENT; HEART LEFT VENTRICLE OUTFLOW TRACT; HEART RIGHT VENTRICLE OUTFLOW TRACT; HEART VENTRICLE SEPTUM DEFECT; MESODERM; MOUSE; MUTAGENESIS; NEURAL CREST; NONHUMAN; PHARYNX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ABNORMALITIES; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGICAL MODEL; BRANCHIAL ARCH; CARDIOVASCULAR SYSTEM; CELL LINEAGE; CYTOLOGY; EMBRYOLOGY; FEMALE; GENETICS; KNOCKOUT MOUSE; MAMMALIAN EMBRYO; METABOLISM; MORPHOGENESIS; MUTATION; NEWBORN; PATHOLOGY; PHENOTYPE; PREGNANCY; STEM CELL; THYMUS; VASCULARIZATION;

ANIMALS; ANIMALS, NEWBORN; BRANCHIAL REGION; CARDIOVASCULAR SYSTEM; CELL LINEAGE; EMBRYO, MAMMALIAN; FEMALE; FIBRONECTINS; INTEGRIN ALPHA5BETA1; LIM-HOMEODOMAIN PROTEINS; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MORPHOGENESIS; MUTATION; NEURAL CREST; ORGAN SPECIFICITY; PHARYNX; PHENOTYPE; PREGNANCY; SIGNAL TRANSDUCTION; STEM CELLS; T-BOX DOMAIN PROTEINS; THYMUS GLAND; TRANSCRIPTION FACTORS;

EID: 84952864194     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2015.09.016     Document Type: Article

References (68)

1. Adams R.H., Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell. Biol. 2007, 8:464-478.
2. Astrof S. Interactions between neural crest-derived cells and extracellular microenvironment during cardiovascular development. Extracellular Matrix in Development 2013, 105-131. Springer Verlag, Berlin. D.W. Desimone, R.P. Mecham (Eds.).
3. Astrof S., Hynes R.O. Fibronectins in vascular morphogenesis. Angiogenesis 2009, 12:165-175.
4. Bressan M., Davis P., Timmer J., Herzlinger D., Mikawa T. Notochord-derived BMP antagonists inhibit endothelial cell generation and network formation. Dev. Biol. 2009, 326:101-111.
5. 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.
6. Calmont A., Ivins S., Van Bueren K.L., Papangeli I., Kyriakopoulou V., Andrews W.D., Martin J.F., Moon A.M., Illingworth E.A., Basson M.A., Scambler P.J. Tbx1 controls cardiac neural crest cell migration during arch artery development by regulating Gbx2 expression in the pharyngeal ectoderm. Development 2009, 136:3173-3183.
7. Culver J.C., Dickinson M.E. The effects of hemodynamic force on embryonic development. Microcirculation 2010, 17:164-178.
8. Engleka K.A., Manderfield L.J., Brust R.D., Li L., Cohen A., Dymecki S.M., Epstein J.A. Islet1 derivatives in the heart are of both neural crest and second heart field origin. Circ. Res. 2012, 110:922-926.
9. Foster K., Sheridan J., Veiga-Fernandes H., Roderick K., Pachnis V., Adams R., Blackburn C., Kioussis D., Coles M. Contribution of neural crest-derived cells in the embryonic and adult thymus. J. Immunol. 2008, 180:3183-3189.
10. Gao Z., Kim G.H., Mackinnon A.C., Flagg A.E., Bassett B., Earley J.U., Svensson E.C. Ets1 is required for proper migration and differentiation of the cardiac neural crest. Development 2010, 137:1543-1551.
11. Garriock R.J., Czeisler C., Ishii Y., Navetta A.M., Mikawa T. An anteroposterior wave of vascular inhibitor downregulation signals aortae fusion along the embryonic midline axis. Development 2010, 137:3697-3706.
12. George E.L., Baldwin H.S., Hynes R.O. Fibronectins are essential for heart and blood vessel morphogenesis but are dispensable for initial specification of precursor cells. Blood 1997, 90:3073-3081.
13. George E.L., Georges-Labouesse E.N., Patel-King R.S., Rayburn H., Hynes R.O. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 1993, 119:1079-1091.
14. Giancotti F.G., Tarone G. Positional control of cell fate through joint integrin/receptor protein kinase signaling. Annu. Rev. Cell. Dev. Biol. 2003, 19:173-206.
15. Gitler A.D., Lu M.M., Epstein J.A. PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. Dev. Cell. 2004, 7:107-116.
16. Goh K.L., Yang J.T., Hynes R.O. Mesodermal defects and cranial neural crest apoptosis in alpha5 integrin-null embryos. Development 1997, 124:4309-4319.
17. Haack H., Hynes R.O. Integrin receptors are required for cell survival and proliferation during development of the peripheral glial lineage. Dev. Biol. 2001, 233:38-55.
18. High F.A., Epstein J.A. The multifaceted role of Notch in cardiac development and disease. Nat. Rev. Genet. 2008, 9:49-61.
19. High F.A., Jain R., Stoller J.Z., Antonucci N.B., Lu M.M., Loomes K.M., Kaestner K.H., Pear W.S., Epstein J.A. Murine Jagged1/Notch signaling in the second heart field orchestrates Fgf8 expression and tissue-tissue interactions during outflow tract development. J. Clin. Invest. 2009, 119:1986-1996.
20. Huang D.W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
21. Hutson M.R., Kirby M.L. Model systems for the study of heart development and disease. Cardiac neural crest and conotruncal malformations. Semin. Cell Dev. Biol. 2007, 18:101-110.
22. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
23. Hynes R.O. The extracellular matrix: not just pretty fibrils. Science 2009, 326:1216-1219.
24. Hynes R.O. Evolution: The evolution of metazoan extracellular matrix. J. Cell Biol. 2012, 196:671-679.
25. Hynes R.O., Zhao Q. The evolution of cell adhesion. J. Cell Biol. 2000, 150:F89-F96.
26. Kirby M.L. Cardiac Development 2007, Oxford University Press, New York.
27. Le Douarin N.M., Jotereau F.V. Tracing of cells of the avian thymus through embryonic life in interspecific chimeras. J. Exp. Med. 1975, 142:17-40.
28. Li P., Pashmforoush M., Sucov H.M. Mesodermal retinoic acid signaling regulates endothelial cell coalescence in caudal pharyngeal arch artery vasculogenesis. Dev. Biol. 2012, 361:116-124.
29. Liang D., Wang X., Mittal A., Dhiman S., Hou S.Y., Degenhardt K., Astrof S. Mesodermal expression of integrin alpha5beta1 regulates neural crest development and cardiovascular morphogenesis. Dev. Biol. 2014, 395:232-244.
30. Liao J., Kochilas L., Nowotschin S., Arnold J.S., Aggarwal V.S., Epstein J.A., Brown M.C., Adams J., Morrow B.E. Full spectrum of malformations in velo-cardio-facial syndrome/DiGeorge syndrome mouse models by altering Tbx1 dosage. Hum. Mol. Genet. 2004, 13:1577-1585.
31. Lindsay E.A., Baldini A. Recovery from arterial growth delay reduces penetrance of cardiovascular defects in mice deleted for the DiGeorge syndrome region. Hum. Mol. Genet. 2001, 10:997-1002.
32. 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 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 2001, 410:97-101.
33. Lucitti J.L., Jones E.A., Huang C., Chen J., Fraser S.E., Dickinson M.E. Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 2007, 134:3317-3326.
34. Luo Y., Ferreira-Cornwell M., Baldwin H., Kostetskii I., Lenox J., Lieberman M., Radice G. Rescuing the N-cadherin knockout by cardiac-specific expression of N- or E-cadherin. Development 2001, 128:459-469.
35. 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.
36. Martino M.M., Hubbell J.A. The 12th-14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain. FASEB J. 2010, 24:4711-4721.
37. Meadows S.M., Fletcher P.J., Moran C., Xu K., Neufeld G., Chauvet S., Mann F., Krieg P.A., Cleaver O. Integration of repulsive guidance cues generates avascular zones that shape mammalian blood vessels. Circ. Res. 2012, 110:34-46.
38. Merscher S., Funke B., Epstein J.A., Heyer J., Puech A., Lu M.M., Xavier R.J., Demay M.B., Russell R.G., Factor S., Tokooya K., Jore B.S., Lopez M., Pandita R.K., Lia M., Carrion D., Xu H., Schorle H., Kobler J.B., Scambler P., Wynshaw-Boris A., Skoultchi A.I., Morrow B.E., Kucherlapati R. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 2001, 104:619-629.
39. Mittal A., Pulina M., Hou S., Astrof S. Fibronectin and integrin alpha 5 play requisite roles in cardiac morphogenesis. Dev. Biol. 2013, 381:73-82.
40. Mittal A., Pulina M., Hou S.Y., Astrof S. Fibronectin and integrin alpha 5 play essential roles in the development of the cardiac neural crest. Mech. Dev. 2010, 127:472-484.
41. Miyamoto S., Teramoto H., Gutkind J.S., Yamada K.M. Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors. J. Cell Biol. 1996, 135:1633-1642.
42. Moon A. Mouse models of congenital cardiovascular disease. Curr. Top. Dev. Biol. 2008, 84:171-248.
43. Moon A.M. Mouse models for investigating the developmental basis of human birth defects. Pediatr. Res. 2006, 59:749-755.
44. Muzumdar M.D., Tasic B., Miyamichi K., Li L., Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007, 45:593-605.
45. Papangeli I., Scambler P. The 22q11 deletion: DiGeorge and velocardiofacial syndromes and the role of TBX1. Wiley Interdiscip. Rev. Dev. Biol. 2013, 2:393-403.
46. Papangeli I., Scambler P.J. Tbx1 genetically interacts with the transforming growth factor-beta/bone morphogenetic protein inhibitor Smad7 during great vessel remodeling. Circ. Res. 2013, 112:90-102.
47. 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.
48. Pulina M., Liang D., Astrof S. Shape and position of the node and notochord along the bilateral plane of symmetry are regulated by cell-extracellular matrix interactions. Biol. Open. 2014, 3:583-590.
49. Pulina M.V., Hou S.Y., Mittal A., Julich D., Whittaker C.A., Holley S.A., Hynes R.O., Astrof S. Essential roles of fibronectin in the development of the left-right embryonic body plan. Dev. Biol. 2011, 354:208-220.
50. Roger V.L., Go A.S., Lloyd-Jones D.M., Adams R.J., Berry J.D., Brown T.M., Carnethon M.R., Dai S., de Simone G., Ford E.S., Fox C.S., Fullerton H.J., Gillespie C., Greenlund K.J., Hailpern S.M., Heit J.A., Ho P.M., Howard V.J., Kissela B.M., Kittner S.J., Lackland D.T., Lichtman J.H., Lisabeth L.D., Makuc D.M., Marcus G.M., Marelli A., Matchar D.B., McDermott M.M., Meigs J.B., Moy C.S., Mozaffarian D., Mussolino M.E., Nichol G., Paynter N.P., Rosamond W.D., Sorlie P.D., Stafford R.S., Turan T.N., Turner M.B., Wong N.D., Wylie-Rosett J. Heart disease and stroke statistics-2011 update: a report from the American Heart Association. Circulation 2011, 123:e18-e209.
51. Saga Y., Kitajima S., Miyagawa-Tomita S. Mesp1 expression is the earliest sign of cardiovascular development. Trends Cardiovasc. Med. 2000, 10:345-352.
52. Sakai T., Johnson K.J., Murozono M., Sakai K., Magnuson M.A., Wieloch T., Cronberg T., Isshiki A., Erickson H.P., Fassler R. Plasma fibronectin supports neuronal survival and reduces brain injury following transient focal cerebral ischemia but is not essential for skin-wound healing and hemostasis. Nat. Med. 2001, 7:324-330.
53. Schwartz M.A. Integrins and extracellular matrix in mechanotransduction. Cold Spring Harb. Perspect. Biol. 2010, 2:a005066.
54. Schwartz M.A., Assoian R.K. Integrins and cell proliferation: regulation of cyclin-dependent kinases via cytoplasmic signaling pathways. J. Cell Sci. 2001, 114:2553-2560.
55. Takahashi S., Leiss M., Moser M., Ohashi T., Kitao T., Heckmann D., Pfeifer A., Kessler H., Takagi J., Erickson H.P., Fassler R. The RGD motif in fibronectin is essential for development but dispensable for fibril assembly. J. Cell Biol. 2007, 178:167-178.
56. Turlo K.A., Noel O.D., Vora R., Larussa M., Fassler R., Hall-Glenn F., Iruela-Arispe M.L. An essential requirement for beta1 integrin in the assembly of extracellular matrix proteins within the vascular wall. Dev. Biol. 2012, 365:23-35.
57. Turner C.J., Badu-Nkansah K., Crowley D., van der Flier A., Hynes R.O. Integrin-alpha5beta1 is not required for mural cell functions during development of blood vessels but is required for lymphatic-blood vessel separation and lymphovenous valve formation. Dev. Biol. 2014, 392:381-392.
58. Turner C.J., Badu-Nkansah K., Crowley D., van der Flier A., Hynes R.O. alpha5 and alphav integrins cooperate to regulate vascular smooth muscle and neural crest functions in vivo. Development 2015, 142:797-808.
59. van der Flier A., Badu-Nkansah K., Whittaker C.A., Crowley D., Bronson R.T., Lacy-Hulbert A., Hynes R.O. Endothelial alpha5 and alphav integrins cooperate in remodeling of the vasculature during development. Development 2010, 137:2439-2449.
60. Villegas S.N., Barrios-Llerena M.E., Pulina M., Hadjantonakis A.K., Le Bihan T., Astrof S., Brickman J.M. PI3K/Akt1 signalling specifies foregut precursors by generating regionalized extra-cellular matrix. eLife 2013, 2:e00806.
61. Whittaker C.A., Bergeron K.F., Whittle J., Brandhorst B.P., Burke R.D., Hynes R.O. The echinoderm adhesome. Dev. Biol. 2006, 300:252-266.
62. Whittaker C.A., Hynes R.O. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell. 2002, 13:3369-3387.
63. Wickstrom S.A., Radovanac K., Fassler R. Genetic analyses of integrin signaling. Cold Spring Harb. Perspect. Biol. 2011, 3.
64. Wijelath E.S., Murray J., Rahman S., Patel Y., Ishida A., Strand K., Aziz S., Cardona C., Hammond W.P., Savidge G.F., Rafii S., Sobel M. Novel vascular endothelial growth factor binding domains of fibronectin enhance vascular endothelial growth factor biological activity. Circ. Res. 2002, 91:25-31.
65. Yang J.T., Bader B.L., Kreidberg J.A., Ullman-Cullere M., Trevithick J.E., Hynes R.O. Overlapping and independent functions of fibronectin receptor integrins in early mesodermal development. Dev. Biol. 1999, 215:264-277.
66. Yang J.T., Rayburn H., Hynes R.O. Embryonic mesodermal defects in alpha 5 integrin-deficient mice. Development 1993, 119:1093-1105.
67. Zhang Y., Singh M.K., Degenhardt K.R., Lu M.M., Bennett J., Yoshida Y., Epstein J.A. Tie2Cre-mediated inactivation of plexinD1 results in congenital heart, vascular and skeletal defects. Dev. Biol. 2009, 325:82-93.
68. Zhang Z., Huynh T., Baldini A. Mesodermal expression of Tbx1 is necessary and sufficient for pharyngeal arch and cardiac outflow tract development. Development 2006, 133:3587-3595.