Angiogenic factors stimulate tubular branching morphogenesis of sonic hedgehog-deficient lungs

Developmental Biology

Volumn 303, Issue 2, 2007, Pages 514-526

  van Tuyl, Minke ^a,b   Groenman, Freek ^a,b   Wang, Jinxia ^a   Kuliszewski, Maciek ^a   Liu, Jason ^a   Tibboel, Dick ^b   Post, Martin ^a  

^a CANADIAN INSTITUTES OF HEALTH RESEARCH   (Canada)

^b SOPHIA CHILDREN S HOSPITAL   (Netherlands)

Author keywords

Angiogenesis; Angiopoietins; Fgf2; Lung development; Vasculogenesis; Vegf

Indexed keywords

ANGIOGENIC FACTOR; ANGIOPOIETIN 1; ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; BETA GALACTOSIDASE; CD31 ANTIGEN; FIBROBLAST GROWTH FACTOR 2; MESSENGER RNA; SONIC HEDGEHOG PROTEIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 2;

AIRWAY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DETERIORATION; DOWN REGULATION; EMBRYO; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG BLOOD VESSEL; LUNG DEVELOPMENT; MORPHOGENESIS; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULARIZATION; WILD TYPE;

ERINACEIDAE; MUS;

EID: 33847665111     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.11.029     Document Type: Article

References (65)

1. Apelqvist A., Ahlgren U., and Edlund H. Sonic hedgehog directs specialized mesoderm differentiation in the intestine and pancreas. Curr. Biol. 7 (1997) 801-804
2. Bellusci S., Grindley J., Emoto H., et al. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124 (1997) 4867-4878
3. Bellusci S., Furuta Y., Rush M.G., et al. Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124 (1997) 53-63
4. Bikfalvi A., Klein S., Pintucci G., et al. Biological roles of fibroblast growth factor-2. Endocr. Rev. 18 (1997) 26-45
5. Brown L.A., Rodaway A.R., Schilling T.F., et al. Insights into early vasculogenesis revealed by expression of the ETS-domain transcription factor Fli-1 in wild-type and mutant zebrafish embryos. Mech. Dev. 90 (2000) 237-252
6. Carmeliet P., Ferreira V., Breier G., et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380 (1996) 435-439
7. Chiang C., Litingtung Y., Lee E., et al. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383 (1996) 407-413
8. deMello D.E., Sawyer D., Galvin N., et al. Early fetal development of lung vasculature. Am. J. Respir. Cell Mol. Biol. 16 (1997) 568-581
9. Dumont D.J., Gradwohl G., Fong G.H., et al. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev. 8 (1994) 1897-1909
10. Elson D.A., Thurston G., Huang L.E., et al. Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1alpha. Genes Dev. 15 (2001) 2520-2532
11. Ferrara N., Carver-Moore K., Chen H., et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380 (1996) 439-442
12. Galambos C., Ng Y.S., Ali A., Noguchi A., et al. Defective pulmonary development in the absence of heparin-binding vascular endothelial growth factor isoforms. Am. J. Respir. Cell Mol. Biol. 27 (2002) 194-203
13. Gerber H.P., Hillan K.J., Ryan A.M., et al. VEGF is required for growth and survival in neonatal mice. Development 126 (1999) 1149-1159
14. Gonzalez A.M., Hill D.J., Logan A., et al. Distribution of fibroblast growth factor (FGF)-2 and FGF receptor-1 messenger RNA expression and protein presence in the mid-trimester human fetus. Pediatr. Res. 39 (1996) 375-385
15. Han R.N., Liu J., Tanswell A.K., et al. Expression of basic fibroblast growth factor and receptor: immunolocalization studies in developing rat fetal lung. Pediatr. Res. 31 (1992) 435-440
16. Holash J., Wiegand S.J., and Yancopoulos G.D. New model of tumor angiogenesis: dynamic balance between vessel regression and growth mediated by angiopoietins and VEGF. Oncogene 18 (1999) 5356-5362
17. Jakkula M., Le Cras T.D., Gebb S., et al. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am. J. Physiol.: Lung Cell. Mol. Physiol. 279 (2002) L600-L607
18. Kanda S., Mochizuki Y., Suematsu T., et al. Sonic hedgehog induces capillary morphogenesis by endothelial cells through phosphoinositide 3-kinase. J. Biol. Chem. 278 (2003) 8244-8249
19. Krishnan V., Pereira F.A., Qiu Y., et al. Mediation of Sonic hedgehog-induced expression of COUP-TFII by a protein phosphatase. Science 278 (1997) 1947-1950
20. Lammert E., Cleaver O., and Melton D. Role of endothelial cells in early pancreas and liver development. Mech. Dev. 120 (2003) 59-64
21. Lavine K.J., White A.C., Park C., et al. Fibroblast growth factor signals regulate a wave of Hedgehog activation that is essential for coronary vascular development. Genes Dev. 20 (2006) 1651-1666
22. Lawson N.D., Vogel A.M., and Weinstein B.M. sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev. Cell 3 (2002) 127-136
23. Lebeche D., Malpel S., and Cardoso W.V. Fibroblast growth factor interactions in the developing lung. Mech. Dev. 86 (1999) 125-136
24. Le Cras T.D., Markham N.E., Tuder R.M., et al. Treatment of newborn rats with a VEGF receptor inhibitor causes pulmonary hypertension and abnormal lung structure. Am. J. Physiol.: Lung Cell. Mol. Physiol. 283 (2002) L555-L562
25. Litingtung Y., Lei L., Westphal H., et al. Sonic hedgehog is essential to foregut development. Nat. Genet. 20 (1998) 58-61
26. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(- Delta Delta C(T)) Method. Methods 25 (2001) 402-408
27. Madison B.B., Braunstein K., Kuizon E., et al. Epithelial hedgehog signals pattern the intestinal crypt-villus axis. Development 132 (2005) 279-289
28. Maisonpierre P.C., Suri C., Jones P.F., et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277 (1997) 55-60
29. Malpel S., Mendelsohn C., and Cardoso W.V. Regulation of retinoic acid signaling during lung morphogenesis. Development 127 (2000) 3057-3067
30. Matsumoto K., Yoshitomi H., Rossant J., et al. Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294 (2001) 559-563
31. McGrath-Morrow S.A., Cho C., Zhen L., et al. Vascular endothelial growth factor receptor 2 blockade disrupts postnatal lung development. Am. J. Respir. Cell Mol. Biol. 32 (2005) 420-427
32. Miller L.A., Wert S.E., and Whitsett J.A. Immunolocalization of sonic hedgehog (Shh) in developing mouse lung. J. Histochem. Cytochem. 49 (2001) 1593-1604
33. Miller L.A., Wert S.E., Clark J.C., et al. Role of Sonic hedgehog in patterning of tracheal-bronchial cartilage and the peripheral lung. Dev. Dyn. 231 (2004) 57-71
34. Ng Y.S., Rohan R., Sunday M.E., et al. Differential expression of VEGF isoforms in mouse during development and in the adult. Dev. Dyn. 220 (2001) 112-121
35. Nogawa H., and Ito T. Branching morphogenesis of embryonic mouse lung epithelium in mesenchyme-free culture. Development 121 (1995) 1015-1022
36. Orr-Urtreger A., Bedford M.T., Burakova T., et al. Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev. Biol. 158 (1993) 475-486
37. Parera M.C., van Dooren M., van Kempen M., et al. Distal angiogenesis: a new concept for lung vascular morphogenesis. Am. J. Physiol.: Lung Cell. Mol. Physiol. 288 (2005) L141-L149
38. Park W.Y., Miranda B., Lebeche D., et al. FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev. Biol. 201 (1998) 125-134
39. Pepicelli C.V., Lewis P.M., and McMahon A.P. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr. Biol. 8 (1998) 1083-1086
40. Pereira F.A., Qiu Y., Tsai M.J., Tsai S.Y., et al. Chicken ovalbumin upstream promoter transcription factor (COUP-TF): expression during mouse embryogenesis. J. Steroid Biochem. Mol. Biol. 53 (1995) 503-508
41. Pereira F.A., Qiu Y., Zhou G., et al. The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart development. Genes Dev. 13 (1999) 1037-1049
42. Pola R., Ling L.E., Silver M., et al. The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat. Med. 7 (2001) 706-711
43. Pola R., Ling L.E., Aprahamian T.R., et al. Postnatal recapitulation of embryonic hedgehog pathway in response to skeletal muscle ischemia. Circulation 108 (2003) 479-485
44. Powell P.P., Wang C.C., Horinouchi H., et al. Differential expression of fibroblast growth factor receptors 1 to 4 and ligand genes in late fetal and early postnatal rat lung. Am. J. Respir. Cell Mol. Biol. 19 (1998) 563-572
45. Risau W. Mechanisms of angiogenesis. Nature 386 (1997) 671-674
46. Risau W., and Flamme I. Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11 (1995) 73-91
47. Rowitch D.H., S-Jacques B., Lee S.M., et al. Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells. Annu. Rev. Cell Dev. Biol. 19 (1999) 8954-8965
48. Sato T.N., Tozawa Y., Deutsch U., et al. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376 (1995) 70-74
49. Schachtner S.K., Wang Y., and Scott Baldwin H. Qualitative and quantitative analysis of embryonic pulmonary vessel formation. Am. J. Respir. Cell Mol. Biol. 22 (2000) 157-165
50. Schlaeger T.M., Bartunkova S., Lawitts J.A., et al. Uniform vascular-endothelial-cell-specific gene expression in both embryonic and adult transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 94 (1998) 3058-3063
51. Schwarz M.A., Zhang F., Gebb S., et al. Endothelial monocyte activating polypeptide II inhibits lung neovascularization and airway epithelial morphogenesis. Mech. Dev. 95 (2000) 123-132
52. Seghezzi G., Patel S., Ren C.J., et al. Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J. Cell Biol. 141 (1998) 1659-1673
53. Shalaby F., Rossant J., Yamaguchi T.P., et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376 (1995) 62-66
54. Suri C., Jones P.F., Patan S., et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87 (1996) 1171-1180
55. Suri C., McClain J., Thurston G., McDonald D.M., et al. Increased vascularization in mice overexpressing angiopoietin-1. Science 282 (1998) 468-471
56. Tanswell A.K., Han R.N., Jassal D., et al. The response of small vessel endothelial cells from fetal rat lung to growth factors. J. Dev. Physiol. 15 (1991) 199-209
57. Thurston G., Suri C., Smith K., et al. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 286 (1999) 2511-2514
58. Tille J.C., Wood J., Mandriota S.J., et al. Vascular endothelial growth factor (VEGF) receptor-2 antagonists inhibit VEGF- and basic fibroblast growth factor-induced angiogenesis in vivo and in vitro. J. Pharmacol. Exp. Ther. 299 (2001) 1073-1085
59. Tsai S.Y., and Tsai M.J. Chick ovalbumin upstream promoter-transcription factors (COUP-TFs): coming of age. Endocr. Rev. 18 (1997) 229-240
60. Unger S., Copland I., Tibboel D., et al. Down-regulation of sonic hedgehog expression in pulmonary hypoplasia is associated with congenital diaphragmatic hernia. Am. J. Pathol. 162 (2003) 547-555
61. Van Tuyl M., and Post M. From fruitflies to mammals: mechanisms of signalling via the Sonic hedgehog pathway in lung development. Respir. Res. 1 (2000) 30-35
62. Witzenbichler B., Maisonpierre P.C., Jones P., et al. Chemotactic properties of angiopoietin-1 and -2, ligands for the endothelial-specific receptor tyrosine kinase Tie2. J. Biol. Chem. 273 (1998) 18514-18521
63. Yancopoulos G.D., Klagsbrun M., and Folkman J. Vasculogenesis, angiogenesis, and growth factors: ephrins enter the fray at the border. Cell 93 (1998) 661-664
64. Yancopoulos G.D., Davis S., Gale N.W., et al. Vascular-specific growth factors and blood vessel formation. Nature 407 (2000) 242-282
65. Zhang X., Ibrahimi O.A., Olsen S.K., et al. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 281 (2006) 15694-15700