Interactions Between Neural Crest-Derived Cells and Extracellular Microenvironment During Cardiovascular Development

Biology of Extracellular Matrix

Volumn Part F2617, Issue , 2013, Pages 105-131

  Astrof, Sophie ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Arch Artery; Cardiac Neural Crest; Neural Crest; Neural Crest Cell; Pharyngeal Arch

Indexed keywords

EID: 84881557216     PISSN: 08873224     EISSN: 21911959     Source Type: Book Series    
DOI: 10.1007/978-3-642-35935-4_5     Document Type: Chapter

References (125)

1. Arrington CB, Yost HJ (2009) Extra-embryonic syndecan 2 regulates organ primordia migration and fibrillogenesis throughout the zebrafish embryo. Development 136:3143–3152
2. Astrof S, Hynes RO (2009) Fibronectins in vascular morphogenesis. Angiogenesis 12:165–175
3. Astrof NS, Salas A, Shimaoka M, Chen J, Springer TA (2006) Importance of force linkage in mechanochemistry of adhesion receptors. Biochemistry 45:15020–15028
4. Astrof S, Crowley D, Hynes RO (2007) Multiple cardiovascular defects caused by the absence of alternatively spliced segments of fibronectin. Dev Biol 311:11–24
5. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P, Engel J, Engvall E, Hohenester E, Jones JC et al (2005) A simplified laminin nomenclature. Matrix Biol 24:326–332
6. Breau MA, Pietri T, Eder O, Blanche M, Brakebusch C, Fassler R, Thiery JP, Dufour S (2006) Lack of beta1 integrins in enteric neural crest cells leads to a Hirschsprung-like phenotype. Development 133:1725–1734
7. Cai CL, Martin JC, Sun Y, Cui L, Wang L, Ouyang K, Yang L, Bu L, Liang X, Zhang X et al (2008) A myocardial lineage derives from Tbx18 epicardial cells. Nature 454:104–108
8. Calmont A, Ivins S, Van Bueren KL, Papangeli I, Kyriakopoulou V, Andrews WD, Martin JF, Moon AM, Illingworth EA, Basson MA et al (2009) Tbx1 controls cardiac neural crest cell migration during arch artery development by regulating Gbx2 expression in the pharyngeal ectoderm. Development 136:3173–3183
9. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C et al (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435–439
10. Carmona-Fontaine C, Matthews HK, Kuriyama S, Moreno M, Dunn GA, Parsons M, Stern CD, Mayor R (2008) Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456:957–961
11. Carmona-Fontaine C, Theveneau E, Tzekou A, Tada M, Woods M, Page KM, Parsons M, Lambris JD, Mayor R (2011) Complement fragment C3a controls mutual cell attraction during collective cell migration. Dev Cell 21:1026–1037
12. Chan WY, Cheung CS, Yung KM, Copp AJ (2004) Cardiac neural crest of the mouse embryo: axial level of origin, migratory pathway and cell autonomy of the splotch (Sp2H) mutant effect. Development 131:3367–3379
13. Chen TT, Luque A, Lee S, Anderson SM, Segura T, Iruela-Arispe ML (2010) Anchorage of VEGF to the extracellular matrix conveys differential signaling responses to endothelial cells. J Cell Biol 188:595–609
14. Coles EG, Gammill LS, Miner JH, Bronner-Fraser M (2006) Abnormalities in neural crest cell migration in laminin alpha5 mutant mice. Dev Biol 289:218–228
15. Cooley MA, Kern CB, Fresco VM, Wessels A, Thompson RP, McQuinn TC, Twal WO, Mjaatvedt CH, Drake CJ, Argraves WS (2008) Fibulin-1 is required for morphogenesis of neural crestderived structures. Dev Biol 319:336–345
16. Copp AJ, Carvalho R, Wallace A, Sorokin L, Sasaki T, Greene ND, Ybot-Gonzalez P (2011) Regional differences in the expression of laminin isoforms during mouse neural tube development. Matrix Biol 30:301–309
17. Costa-Silva B, da Costa MC, Melo FR, Neves CM, Alvarez-Silva M, Calloni GW, Trentin AG (2009) Fibronectin promotes differentiation of neural crest progenitors endowed with smooth muscle cell potential. Exp Cell Res 315:955–967
18. Costell M, Carmona R, Gustafsson E, Gonzalez-Iriarte M, Fassler R, Munoz-Chapuli R (2002) Hyperplastic conotruncal endocardial cushions and transposition of great arteries in perlecannull mice. Circ Res 91:158–164
19. De Langhe SP, Sala FG, Del Moral PM, Fairbanks TJ, Yamada KM, Warburton D, Burns RC, Bellusci S (2005) Dickkopf-1 (DKK1) reveals that fibronectin is a major target of Wnt signaling in branching morphogenesis of the mouse embryonic lung. Dev Biol 277:316–331
20. Delannet M, Martin F, Bossy B, Cheresh DA, Reichardt LF, Duband JL (1994) Specific roles of the alpha V beta 1, alpha V beta 3 and alpha V beta 5 integrins in avian neural crest cell adhesion and migration on vitronectin. Development 120:2687–2702
21. Duband JL, Thiery JP (1987) Distribution of laminin and collagens during avian neural crest development. Development 101:461–478
22. Dutt S, Kleber M, Matasci M, Sommer L, Zimmermann DR (2006) Versican V0 and V1 guide migratory neural crest cells. J Biol Chem 281:12123–12131
23. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689
24. Erickson CA, Tosney KW, Weston JA (1980) Analysis of migratory behavior of neural crest and fibroblastic cells in embryonic tissues. Dev Biol 77:142–156
25. Feiner L, Webber AL, Brown CB, Lu MM, Jia L, Feinstein P, Mombaerts P, Epstein JA, Raper JA (2001) Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption. Development 128:3061–3070
26. Ffrench-Constant C, Hynes RO (1989) Alternative splicing of fibronectin is temporally and spatially regulated in the chicken embryo. Development 106:375–388
27. Ffrench-Constant C, Van de Water L, Dvorak HF, Hynes RO (1989) Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat. J Cell Biol 109:903–914
28. Fontana L, Chen Y, Prijatelj P, Sakai T, Fassler R, Sakai LY, Rifkin DB (2005) Fibronectin is required for integrin alphavbeta6-mediated activation of latent TGF-beta complexes containing LTBP-1. FASEB J 19:1798–1808
29. Fournier-Thibault C, Blavet C, Jarov A, Bajanca F, Thorsteinsdottir S, Duband JL (2009) Sonic hedgehog regulates integrin activity, cadherin contacts, and cell polarity to orchestrate neural tube morphogenesis. J Neurosci 29:12506–12520
30. Fuchs S, Herzog D, Sumara G, Buchmann-Moller S, Civenni G, Wu X, Chrostek-Grashoff A, Suter U, Ricci R, Relvas JB et al (2009) Stage-specific control of neural crest stem cell proliferation by the small rho GTPases Cdc42 and Rac1. Cell Stem Cell 4:236–247
31. Gammill LS, Roffers-Agarwal J (2010) Division of labor during trunk neural crest development. Dev Biol 344:555–565
32. Gammill LS, Gonzalez C, Gu C, Bronner-Fraser M (2006) Guidance of trunk neural crest migration requires neuropilin 2/semaphorin 3F signaling. Development 133:99–106
33. Gammill LS, Gonzalez C, Bronner-Fraser M (2007) Neuropilin 2/semaphorin 3F signaling is essential for cranial neural crest migration and trigeminal ganglion condensation. Dev Neurobiol 67:47–56
34. Giancotti FG, Tarone G (2003) Positional control of cell fate through joint integrin/receptor protein kinase signaling. Annu Rev Cell Dev Biol 19:173–206
35. Gitler AD, Lu MM, Epstein JA (2004) PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. Dev Cell 7:107–116
36. Goddeeris MM, Schwartz R, Klingensmith J, Meyers EN (2007) Independent requirements for Hedgehog signaling by both the anterior heart field and neural crest cells for outflow tract development. Development 134:1593–1604
37. Graham A, Okabe M, Quinlan R (2005) The role of the endoderm in the development and evolution of the pharyngeal arches. J Anat 207:479–487
38. Guris DL, Duester G, Papaioannou VE, Imamoto A (2006) Dose-dependent interaction of Tbx1 and Crkl and locally aberrant RA signaling in a model of del22q11 syndrome. Dev Cell 10:81–92
39. Haack H, Hynes RO (2001) Integrin receptors are required for cell survival and proliferation during development of the peripheral glial lineage. Dev Biol 233:38–55
40. Habashi JP, Doyle JJ, Holm TM, Aziz H, Schoenhoff F, Bedja D, Chen Y, Modiri AN, Judge DP, Dietz HC (2011) Angiotensin II type 2 receptor signaling attenuates aortic aneurysm in mice through ERK antagonism. Science 332:361–365
41. Hari L, Brault V, Kleber M, Lee HY, Ille F, Leimeroth R, Paratore C, Suter U, Kemler R, Sommer L (2002) Lineage-specific requirements of beta-catenin in neural crest development. J Cell Biol 159:867–880
42. Hari L, Miescher I, Shakhova O, Suter U, Chin L, Taketo M, Richardson WD, Kessaris N, Sommer L (2012) Temporal control of neural crest lineage generation by Wnt/beta-catenin signaling. Development 139:2107–2117
43. High FA, Lu MM, Pear WS, Loomes KM, Kaestner KH, Epstein JA (2008) Endothelial expression of the Notch ligand Jagged1 is required for vascular smooth muscle development. Proc Natl Acad Sci USA 105:1955–1959
44. Hirota S, Liu Q, Lee HS, Hossain MG, Lacy-Hulbert A, McCarty JH (2011) The astrocyteexpressed integrin alphavbeta8 governs blood vessel sprouting in the developing retina. Development 138:5157–5166
45. Holm TM, Habashi JP, Doyle JJ, Bedja D, Chen Y, van Erp C, Lindsay ME, Kim D, Schoenhoff F, Cohn RD et al (2011) Noncanonical TGF beta signaling contributes to aortic aneurysm progression in Marfan syndrome mice. Science 332:358–361
46. Honda H, Oda H, Nakamoto T, Honda Z, Sakai R, Suzuki T, Saito T, Nakamura K, Nakao K, Ishikawa T et al (1998) Cardiovascular anomaly, impaired actin bundling and resistance to Srcinduced transformation in mice lacking p130Cas. Nat Genet 19:361–365
47. Horowitz A, Tkachenko E, Simons M (2002) Fibroblast growth factor-specific modulation of cellular response by syndecan-4. J Cell Biol 157:715–725
48. Hutson MR, Sackey FN, Lunney K, Kirby ML (2009) Blocking hedgehog signaling after ablation of the dorsal neural tube allows regeneration of the cardiac neural crest and rescue of outflow tract septation. Dev Biol 335:367–373
49. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687
50. Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326:1216–1219
51. Hynes RO (2012) Evolution: the evolution of metazoan extracellular matrix. J Cell Biol 196:671–679
52. Ikeya M, Lee SM, Johnson JE, McMahon AP, Takada S (1997) Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389:966–970
53. Jain R, Rentschler S, Epstein JA (2010) Notch and cardiac outflow tract development. Ann N Y Acad Sci 1188:184–190
54. Jarov A, Williams KP, Ling LE, Koteliansky VE, Duband JL, Fournier-Thibault C (2003) A dual role for Sonic hedgehog in regulating adhesion and differentiation of neuroepithelial cells. Dev Biol 261:520–536
55. Jones RG, Li X, Gray PD, Kuang J, Clayton F, Samowitz WS, Madison BB, Gumucio DL, Kuwada SK (2006) Conditional deletion of beta1 integrins in the intestinal epithelium causes a loss of Hedgehog expression, intestinal hyperplasia, and early postnatal lethality. J Cell Biol 175:505–514
56. Kaartinen V, Dudas M, Nagy A, Sridurongrit S, Lu MM, Epstein JA (2004) Cardiac outflow tract defects in mice lacking ALK2 in neural crest cells. Development 131:3481–3490
57. Kawasaki T, Kitsukawa T, Bekku Y, Matsuda Y, Sanbo M, Yagi T, Fujisawa H (1999) A requirement for neuropilin-1 in embryonic vessel formation. Development 126:4895–4902
58. Kirby ML, Hutson MR (2010) Factors controlling cardiac neural crest cell migration. Cell Adh Migr 4:609–621
59. Kodo K, Nishizawa T, Furutani M, Arai S, Yamamura E, Joo K, Takahashi T, Matsuoka R, Yamagishi H (2009) GATA6 mutations cause human cardiac outflow tract defects by disrupting semaphorin-plexin signaling. Proc Natl Acad Sci USA 106:13933–13938
60. Kulesa PM, Gammill LS (2010) Neural crest migration: patterns, phases and signals. Dev Biol 344:566–568
61. Le Douarin NM, Kalcheim C (1999) The neural crest, vol 36, 2nd edn. Cambridge University Press, Cambridge
62. Leatherbury L, Gauldin HE, Waldo K, Kirby ML (1990) Microcinephotography of the developing heart in neural crest-ablated chick embryos. Circulation 81:1047–1057
63. Lepore JJ, Mericko PA, Cheng L, Lu MM, Morrisey EE, Parmacek MS (2006) GATA-6 regulates semaphorin 3C and is required in cardiac neural crest for cardiovascular morphogenesis. J Clin Invest 116:929–939
64. Li L, Guris DL, Okura M, Imamoto A (2003) Translocation of CrkL to focal adhesions mediates integrin-induced migration downstream of Src family kinases. Mol Cell Biol 23:2883–2892
65. Liu W, Selever J, Wang D, Lu MF, Moses KA, Schwartz RJ, Martin JF (2004) Bmp4 signaling is required for outflow-tract septation and branchial-arch artery remodeling. Proc Natl Acad Sci USA 101:4489–4494
66. Liu K, Cheng L, Flesken-Nikitin A, Huang L, Nikitin AY, Pauli BU (2010) Conditional knockout of fibronectin abrogates mouse mammary gland lobuloalveolar differentiation. Dev Biol 346:11–24
67. Lohela M, Bry M, Tammela T, Alitalo K (2009) VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol 21:154–165
68. Macatee TL, Hammond BP, Arenkiel BR, Francis L, Frank DU, Moon AM (2003) Ablation of specific expression domains reveals discrete functions of ectoderm-and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130:6361–6374
69. Martino MM, Hubbell JA (2010) The 12th-14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain. FASEB J 24:4711–4721
70. Massague J (1998) TGF-beta signal transduction. Annu Rev Biochem 67:753–791
71. McMahon GA, Dignam JD, Gentry LE (1996) Structural characterization of the latent complex between transforming growth factor beta 1 and beta 1-latency-associated peptide. Biochem J 313(Pt 1):343–351
72. Mittal A, Pulina M, Hou SY, Astrof S (2010) Fibronectin and integrin alpha 5 play essential roles in the development of the cardiac neural crest. Mech Dev 127:472–484
73. Miyamoto S, Teramoto H, Gutkind JS, Yamada KM (1996) 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 135:1633–1642
74. Moon AM (2006) Mouse models for investigating the developmental basis of human birth defects. Pediatr Res 59:749–755
75. Moon AM, Guris DL, Seo JH, Li L, Hammond J, Talbot A, Imamoto A (2006) Crkl deficiency disrupts Fgf8 signaling in a mouse model of 22q11 deletion syndromes. Dev Cell 10:71–80
76. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, Kaminski N, Garat C, Matthay MA et al (1999) The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96:319–328
77. Neptune ER, Frischmeyer PA, Arking DE, Myers L, Bunton TE, Gayraud B, Ramirez F, Sakai LY, Dietz HC (2003) Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nat Genet 33:407–411
78. Nistala H, Lee-Arteaga S, Smaldone S, Siciliano G, Carta L, Ono RN, Sengle G, Arteaga-Solis E, Levasseur R, Ducy P et al (2010) Fibrillin-1 and 2 differentially modulate endogenous TGFbeta and BMP bioavailability during bone formation. J Cell Biol 190:1107–1121
79. Park EJ, Ogden LA, Talbot A, Evans S, Cai CL, Black BL, Frank DU, Moon AM (2006) Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development 133:2419–2433
80. Park EJ, Watanabe Y, Smyth G, Miyagawa-Tomita S, Meyers E, Klingensmith J, Camenisch T, Buckingham M, Moon AM (2008) An FGF autocrine loop initiated in second heart field mesoderm regulates morphogenesis at the arterial pole of the heart. Development 135:3599–3610
81. Peters JH, Hynes RO (1996) Fibronectin isoform distribution in the mouse. I. The alternatively spliced EIIIB, EIIIA, and V segments show widespread codistribution in the developing mouse embryo. Cell Adhes Commun 4:103–125
82. Peters JH, Chen GE, Hynes RO (1996) Fibronectin isoform distribution in the mouse. II. Differential distribution of the alternatively spliced EIIIB, EIIIA, and V segments in the adult mouse. Cell Adhes Commun 4:127–148
83. Pulina MV, Hou SY, Mittal A, Julich D, Whittaker CA, Holley SA, Hynes RO, Astrof S (2011) Essential roles of fibronectin in the development of the left-right embryonic body plan. Dev Biol 354:208–220
84. Rallis C, Pinchin SM, Ish-Horowicz D (2010) Cell-autonomous integrin control of Wnt and Notch signalling during somitogenesis. Development 137:3591–3601
85. Ramsdell AF (2005) Left-right asymmetry and congenital cardiac defects: getting to the heart of the matter in vertebrate left-right axis determination. Dev Biol 288:1–20
86. Rentschler S, Jain R, Epstein JA (2010) Tissue-tissue interactions during morphogenesis of the outflow tract. Pediatr Cardiol 31:408–413
87. Richarte AM, Mead HB, Tallquist MD (2007) Cooperation between the PDGF receptors in cardiac neural crest cell migration. Dev Biol 306:785–796
88. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, Carnethon MR, Dai S, de Simone G, Ford ES et al (2011) Heart disease and stroke statistics–2011 update: a report from the American Heart Association. Circulation 123:e18–e209
89. Rovasio RA, Delouvee A, Yamada KM, Timpl R, Thiery JP (1983) Neural crest cell migration: requirements for exogenous fibronectin and high cell density. J Cell Biol 96:462–473
90. Saoncella S, Echtermeyer F, Denhez F, Nowlen JK, Mosher DF, Robinson SD, Hynes RO, Goetinck PF (1999) Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc Natl Acad Sci USA 96:2805–2810
91. Schwarz Q, Vieira JM, Howard B, Eickholt BJ, Ruhrberg C (2008) Neuropilin 1 and 2 control cranial gangliogenesis and axon guidance through neural crest cells. Development 135:1605–1613
92. Seo JH, Suenaga A, Hatakeyama M, Taiji M, Imamoto A (2009) Structural and functional basis of a role for CRKL in a fibroblast growth factor 8-induced feed-forward loop. Mol Cell Biol 29:3076–3087
93. Serini G, Valdembri D, Zanivan S, Morterra G, Burkhardt C, Caccavari F, Zammataro L, Primo L, Tamagnone L, Logan M et al (2003) Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424:391–397
94. Shi M, Zhu J, Wang R, Chen X, Mi L, Walz T, Springer TA (2011) Latent TGF-beta structure and activation. Nature 474:343–349
95. Sivakumar P, Czirok A, Rongish BJ, Divakara VP, Wang YP, Dallas SL (2006) New insights into extracellular matrix assembly and reorganization from dynamic imaging of extracellular matrix proteins in living osteoblasts. J Cell Sci 119:1350–1360
96. Stalmans I, Lambrechts D, De Smet F, Jansen S, Wang J, Maity S, Kneer P, von der Ohe M, Swillen A, Maes C et al (2003) VEGF: a modifier of the del22q11 (DiGeorge) syndrome? Nat Med 9:173–182
97. Stenzel D, Franco CA, Estrach S, Mettouchi A, Sauvaget D, Rosewell I, Schertel A, Armer H, Domogatskaya A, Rodin S et al (2011a) Endothelial basement membrane limits tip cell formation by inducing Dll4/Notch signalling in vivo. EMBO Rep 12:1135–1143
98. Stenzel D, Lundkvist A, Sauvaget D, Busse M, Graupera M, van der Flier A, Wijelath ES, Murray J, Sobel M, Costell M et al (2011b) Integrin-dependent and-independent functions of astrocytic fibronectin in retinal angiogenesis. Development 138:4451–4463
99. Stottmann RW, Klingensmith J (2011) Bone morphogenetic protein signaling is required in the dorsal neural folds before neurulation for the induction of spinal neural crest cells and dorsal neurons. Dev Dyn 240:755–765
100. Stottmann RW, Choi M, Mishina Y, Meyers EN, Klingensmith J (2004) BMP receptor IA is required in mammalian neural crest cells for development of the cardiac outflow tract and ventricular myocardium. Development 131:2205–2218
101. Strachan LR, Condic ML (2004) Cranial neural crest recycle surface integrins in a substratumdependent manner to promote rapid motility. J Cell Biol 167:545–554
102. Stuhlmiller TJ, Garcia-Castro MI (2012) FGF/MAPK signaling is required in the gastrula epiblast for avian neural crest induction. Development 139:289–300
103. Testaz S, Delannet M, Duband J (1999) Adhesion and migration of avian neural crest cells on fibronectin require the cooperating activities of multiple integrins of the (beta)1 and (beta)3 families. J Cell Sci 112(Pt 24):4715–4728
104. Testaz S, Jarov A, Williams KP, Ling LE, Koteliansky VE, Fournier-Thibault C, Duband JL (2001) Sonic hedgehog restricts adhesion and migration of neural crest cells independently of the Patched-Smoothened-Gli signaling pathway. Proc Natl Acad Sci USA 98:12521–12526
105. Thomas PS, Kim J, Nunez S, Glogauer M, Kaartinen V (2010) Neural crest cell-specific deletion of Rac1 results in defective cell-matrix interactions and severe craniofacial and cardiovascular malformations. Dev Biol 340:613–625
106. Todorovic V, Jurukovski V, Chen Y, Fontana L, Dabovic B, Rifkin DB (2005) Latent TGF-beta binding proteins. Int J Biochem Cell Biol 37:38–41
107. Todorovic V, Frendewey D, Gutstein DE, Chen Y, Freyer L, Finnegan E, Liu F, Murphy A, Valenzuela D, Yancopoulos G et al (2007) Long form of latent TGF-beta binding protein 1 (Ltbp1L) is essential for cardiac outflow tract septation and remodeling. Development 134:3723–3732
108. Toyoda R, Assimacopoulos S, Wilcoxon J, Taylor A, Feldman P, Suzuki-Hirano A, Shimogori T, Grove EA (2010) FGF8 acts as a classic diffusible morphogen to pattern the neocortex. Development 137:3439–3448
109. Toyofuku T, Yoshida J, Sugimoto T, Yamamoto M, Makino N, Takamatsu H, Takegahara N, Suto F, Hori M, Fujisawa H et al (2008) Repulsive and attractive semaphorins cooperate to direct the navigation of cardiac neural crest cells. Dev Biol 321:251–262
110. Trainor PA, Ariza-McNaughton L, Krumlauf R (2002) Role of the isthmus and FGFs in resolving the paradox of neural crest plasticity and prepatterning. Science 295:1288–1291
111. Turlo KA, Noel OD, Vora R, Larussa M, Fassler R, Hall-Glenn F, Iruela-Arispe ML (2012) An essential requirement for beta1 integrin in the assembly of extracellular matrix proteins within the vascular wall. Dev Biol 365:23–35
112. Urness LD, Bleyl SB, Wright TJ, Moon AM, Mansour SL (2011) Redundant and dosage sensitive requirements for Fgf3 and Fgf10 in cardiovascular development. Dev Biol 356:383–397
113. Valdembri D, Caswell PT, Anderson KI, Schwarz JP, Konig I, Astanina E, Caccavari F, Norman JC, Humphries MJ, Bussolino F et al (2009) Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol 7:e25
114. Vallejo-Illarramendi A, Zang K, Reichardt LF (2009) Focal adhesion kinase is required for neural crest cell morphogenesis during mouse cardiovascular development. J Clin Invest 119:2218–2230
115. van den Akker NM, Molin DG, Peters PP, Maas S, Wisse LJ, van Brempt R, van Munsteren CJ, Bartelings MM, Poelmann RE, Carmeliet P et al (2007) Tetralogy of fallot and alterations in vascular endothelial growth factor-A signaling and notch signaling in mouse embryos solely expressing the VEGF120 isoform. Circ Res 100:842–849
116. Veevers-Lowe J, Ball SG, Shuttleworth A, Kielty CM (2011) Mesenchymal stem cell migration is regulated by fibronectin through alpha5beta1-integrin-mediated activation of PDGFR-beta and potentiation of growth factor signals. J Cell Sci 124:1288–1300
117. Vincentz JW, McWhirter JR, Murre C, Baldini A, Furuta Y (2005) Fgf15 is required for proper morphogenesis of the mouse cardiac outflow tract. Genesis 41:192–201
118. Waldo KL, Hutson MR, Stadt HA, Zdanowicz M, Zdanowicz J, Kirby ML (2005) Cardiac neural crest is necessary for normal addition of the myocardium to the arterial pole from the secondary heart field. Dev Biol 281:66–77
119. Wijelath ES, Murray J, Rahman S, Patel Y, Ishida A, Strand K, Aziz S, Cardona C, Hammond WP, Savidge GF et al (2002) Novel vascular endothelial growth factor binding domains of fibronectin enhance vascular endothelial growth factor biological activity. Circ Res 91:25–31
120. Wipff PJ, Hinz B (2008) Integrins and the activation of latent transforming growth factor beta1 – an intimate relationship. Eur J Cell Biol 87:601–615
121. Wurdak H, Ittner LM, Sommer L (2006) DiGeorge syndrome and pharyngeal apparatus development. Bioessays 28:1078–1086
122. Xu X, Francis R, Wei CJ, Linask KL, Lo CW (2006) Connexin 43-mediated modulation of polarized cell movement and the directional migration of cardiac neural crest cells. Development 133:3629–3639
123. Zhang J, Lin Y, Zhang Y, Lan Y, Lin C, Moon AM, Schwartz RJ, Martin JF, Wang F (2008) Frs2alpha-deficiency in cardiac progenitors disrupts a subset of FGF signals required for outflow tract morphogenesis. Development 135:3611–3622
124. Zhang Y, Singh MK, Degenhardt KR, Lu MM, Bennett J, Yoshida Y, Epstein JA (2009) Tie2Cremediated inactivation of plexinD1 results in congenital heart, vascular and skeletal defects. Dev Biol 325:82–93
125. Zou L, Cao S, Kang N, Huebert RC, Shah VH (2012) Fibronectin induces endothelial cell migration through beta1-integrin and Src dependent phosphorylation of fibroblast growth factor receptor-1 at tyrosines 653/654 and 766. J Biol Chem 287(10):7190–7202