Molecular Mechanisms Of Tubulogenesis (original) (raw)

• West, G. B., Brown, J. H. & Enquist, B. J. The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284, 1677–1679 (1999).The authors use mathematical models to explore the importance of branching tubular systems for increasing the metabolic efficiency of organisms as they increased in size during evolution.
  Article CAS PubMed Google Scholar
• Knust, E. Control of epithelial cell shape and polarity. Curr. Opin. Genet. Dev. 10, 471–475 (2000).
  Article CAS PubMed Google Scholar
• Ohno, S. Intercellular junctions and cellular polarity: the PAR–aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr. Opin. Cell Biol. 13, 641–648 (2001).
  Article CAS PubMed Google Scholar
• Bilder, D. PDZ proteins and polarity: functions from the fly. Trends Genet. 17, 511–519 (2001).
  Article CAS PubMed Google Scholar
• Vainio, S. & Lin, Y. Coordinating early kidney development: lessons from gene targeting. Nature Rev. Genet. 3, 533–543 (2002).
  Article CAS PubMed Google Scholar
• Colas, J.-F. & Schoenwolf, G. C. Towards a cellular and molecular understanding of neurulation. Dev. Dyn. 221, 117–145 (2001).A comprehensive review of the cellular and molecular mechanisms underlying neurulation, with emphasis on the chick embryo, and the genetic and environmental factors that are associated with neural-tube defects in mammals.
  Article CAS PubMed Google Scholar
• Bier, E. Drawing lines in the Drosophila wing: initiation of wing vein development. Curr. Opin. Genet. Dev. 10, 393–398 (2000).
  Article CAS PubMed Google Scholar
• Manning, G. & Krasnow, M. A. in The Development of Drosophila melanogaster Vol. 1 (eds Bate, M. & Martinez-Arias, A.) 609–686 (Cold Spring Harbor Laboratory Press, Plainview, New York, 1993).
  Google Scholar
• Buechner, M., Hall, D. H., Bhatt, H. & Hedgecock, E. M. Cystic canal mutants in Caenorhabditis elegans are defective in the apical membrane domain of the renal (excretory) cell. Dev. Biol. 214, 227–241 (1999).
  Article CAS PubMed Google Scholar
• McKeown, C., Praitis, V. & Austin, J. sma-1 encodes a βH-spectrin homolog required for Caenorhabditis elegans morphogenesis. Development 125, 2087–2098 (1998).
  CAS PubMed Google Scholar
• Pasteris, N. G. et al. Isolation and characterization of the faciogenital dysplasia (Aarskog-Scott syndrome) gene: a putative Rho/Rac guanine nucleotide exchange factor. Cell 79, 669–678 (1994).
  Article CAS PubMed Google Scholar
• Suzuki, N. et al. A putative GDP–GTP exchange factor is required for development of the excretory cell in Caenorhabditis elegans. EMBO Rep. 2, 530–535 (2001a).This paper and reference 13 implicate the Rho family of GTPases in controlling lumenal diameter and smoothness, by identifying a GDP–GTP exchange factor (GEF) as a key regulator of these important tubular properties. Rho GTPases might regulate the apical F-actin network, although this is not shown explicitly in this paper.
  Article CAS PubMed PubMed Central Google Scholar
• Gao, J., Estrada, L., Cho, S., Ellis, R. E. & Gorski, J. L. The Caenorhabditis elegans homolog of FGD1, the human Cdc42 GEF gene responsible for faciogenital dysplasia, is critical for excretory cell morphogenesis. Hum. Mol. Genet. 10, 3049–3062 (2001).The authors show that the C. elegans GEF that affects lumenal development of the excretory cell is the homologue of a human GEF that is involved in faciogenital dysplasia. Lumenal development in C. elegans , therefore, provides a model for this human genetic disease.
  Article CAS PubMed Google Scholar
• Lee, S. & Kolodziej, P. A. The plakin Short Stop and the RhoA GTPase are required for E-cadherin-dependent apical surface remodeling during tracheal tube fusion. Development 129, 1509–1520 (2002).The authors investigate the mechanism of de novo lumen formation. They describe the assembly of an F-actin-rich track that is associated with new E-cadherin contacts between tracheal branches. This track directs lumen formation in branch tip cells to connect tracheal branches. RhoA probably functions upstream of Shot to regulate Shot localization to the track and track assembly.
  Article CAS PubMed Google Scholar
• Andrew, D. J., Henderson, K. D. & Seshaiah, P. Salivary gland development in Drosophila melanogaster. Mech. Dev. 92, 5–17 (2000).
  Article CAS PubMed Google Scholar
• Bradley, P. L., Haberman, A. S. & Andrew, D. J. Organ formation in Drosophila: specification and morphogenesis of the salivary gland. Bioessays 23, 901–911 (2001).
  Article CAS PubMed Google Scholar
• Myat, M. M. & Andrew, D. J. Organ shape in the Drosophila salivary gland is controlled by regulated, sequential internalization of the primordia. Development 127, 679–691 (2000).
  CAS PubMed Google Scholar
• Lammel, U. & Saumweber, H. X-linked loci of Drosophila melanogaster causing defects in the morphology of the embryonic salivary glands. Dev. Genes Evol. 210, 525–535 (2000).
  Article CAS PubMed Google Scholar
• Kiehart, D. P., Galbraith, C. G., Edwards, K. A., Rickoll, W. L. & Montague, R. A. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149, 471–490 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Costa, M., Wilson, E. T. & Wieschaus, E. Putative cell signal encoded by the folded gastrulation gene coordinates cell shape changes during Drosophila forkhead gastrulation. Cell 76, 1075–1089 (1994).
  Article CAS PubMed Google Scholar
• Myat, M. M. & Andrew, D. J. Fork head prevents apoptosis and promotes cell shape change during formation of the Drosophila salivary glands. Development 127, 4217–4226 (2000).
  CAS PubMed Google Scholar
• De Felice, M. et al. A mouse model for hereditary thyroid dysgenesis and cleft palate. Nature Genet. 19, 395–398 (1998).
  Article CAS PubMed Google Scholar
• Clifton-Bligh, R. J. et al. Mutation of the gene encoding human TTF-2 associated with thyroid agenesis, cleft palate and choanal atresia. Nature Genet. 19, 399–401 (1998).
  Article CAS PubMed Google Scholar
• Blake, K. J., Myette, G. & Jack, J. ribbon, raw, and zipper have distinct functions in reshaping the Drosophila cytoskeleton. Dev. Genes Evol. 209, 555–559 (1999).
  Article CAS PubMed Google Scholar
• Young, P. E., Richman, A. M., Ketchum, A. S. & Kiehart, D. P. Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 7, 29–41 (1993).
  Article CAS PubMed Google Scholar
• Byars, C. L., Bates, K. L. & Letsou, A. The dorsal–open group gene raw is required for restricted DJNK signaling during closure. Development 126, 4913–4923 (1999).
  CAS PubMed Google Scholar
• Bradley, P. L. & Andrew, D. J. ribbon encodes a novel BTB/POZ protein required for directed cell migration in Drosophila melanogaster. Development 128, 3001–3015. (2001).This paper and reference 29 describe a novel nuclear protein, Ribbon, that is required for tracheal branching. The authors propose that Ribbon regulates the transcription of genes that are involved in steps in cell migration that occur after process extension.
  CAS PubMed Google Scholar
• Shim, K., Blake, K. J., Jack, J. & Krasnow, M. A. The Drosophila ribbon gene encodes a nuclear BTB domain protein that promotes epithelial migration and morphogenesis. Development 128, 4923–4933 (2001).The authors compare the tracheal phenotypes of ribbon mutants to those of mutants in signalling pathways, and also describe the effects of Ribbon on other tubular epithelia, most notably the salivary gland. Given the phenotypic similarities with wingless (wg) mutants, the authors propose that ribbon might function in the wg pathway or parallel to it.
  CAS PubMed Google Scholar
• Metzger, R. J. & Krasnow, M. A. Genetic control of branching morphogenesis. Science 284, 1635–1639 (1999).
  Article CAS PubMed Google Scholar
• Srinivas, S. et al. Expression of green fluorescent protein in the ureteric bud of transgenic mice: a new tool for the analysis of ureteric bud morphogenesis. Dev. Genet. 24, 241–251 (1999).
  Article CAS PubMed Google Scholar
• Makarenkova, H. P. et al. FGF10 is an inducer and Pax6 a competence factor for lacrimal gland development. Development 127, 2563–2572 (2000).
  CAS PubMed Google Scholar
• Weaver, M., Dunn, N. R. & Hogan, B. L. Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127, 2695–2704 (2000).
  CAS PubMed Google Scholar
• Fisher, C. E., Michael, L., Barnett, M. W. & Davies, J. A. Erk MAP kinase regulates branching morphogenesis in the developing mouse kidney. Development 128, 4329–4338 (2001).
  CAS PubMed Google Scholar
• Miura, T. & Shiota, K. Time-lapse observation of branching morphogenesis of the lung bud epithelium in mesenchyme-free culture and its relationship with the localization of actin filaments. Int. J. Dev. Biol. 44, 899–902 (2000).
  CAS PubMed Google Scholar
• Nogawa, H., Morita, K. & Cardoso, W. V. Bud formation precedes the appearance of differential cell proliferation during branching morphogenesis of mouse lung epithelium in vitro. Dev. Dynamics 213, 228–235 (1998).
  Article CAS Google Scholar
• Hogg, N. A. S., Harrison, C. J. & Tickle, C. Lumen formation in the developing mouse mammary gland. J. Embryol. Exp. Morphol. 73, 39–57 (1983).
  CAS PubMed Google Scholar
• Hieda, Y., Iwai, K., Morita, T. & Nakanishi, Y. Mouse embryonic submandibular gland epithelium loses its tissue integrity during early branching morphogenesis. Dev. Dyn. 207, 395–403 (1996).
  Article CAS PubMed Google Scholar
• Nanba, D., Hieda, Y. & Nakanishi, Y. Remodeling of desmosomal and hemidesmosomal adhesion systems during early morphogenesis of mouse pelage hair follicles. J. Invest. Dermatol. 114, 171–177 (2000).
  Article CAS PubMed Google Scholar
• Nanba, D., Nakanishi, Y. & Hieda, Y. Changes in adhesive properties of epithelial cells during early morphogenesis of the mammary gland. Dev. Growth Differ. 43, 535–544 (2001).
  Article CAS PubMed Google Scholar
• Mailleux, A. A. et al. Role of FGF10/FGFR2b signaling during mammary gland development in the mouse embryo. Development 129, 53–60 (2002).Mouse mammary glands develop from five pairs of placodes. Surprisingly, one of the five placodes develops independently of FGF10–FGFR2b, the ligand–receptor combination that directs branching morphogenesis of the other four.
  CAS PubMed Google Scholar
• Hennighausen, L. & Robinson, G. Signaling pathways in mammary gland development. Dev. Cell 1, 467–475 (2001).
  Article CAS PubMed Google Scholar
• Horne-Badovinac, S. et al. Positional cloning of heart and soul reveals multiple roles for PKC lambda in zebrafish organogenesis. Curr. Biol. 11, 1492–1502 (2001).The first characterization of a member of the PAR3–PAR6 complex in vertebrates. The results indicate that, in a rod of cells destined to form a tube, atypical PKC coordinates the movement of F-actin-rich structures towards the rod centre. These structures prefigure lumen formation.
  Article CAS PubMed Google Scholar
• Lengyel, J. A. & Iwaki, D. D. It takes guts: the Drosophila hindgut as a model system for organogenesis. Dev. Biol. 243, 1–19 (2002).A scholarly review of Drosophila hindgut development and the insights it provides into the evolutionarily conserved genetic pathways regulating gut differentiation and morphogenesis.
  Article CAS PubMed Google Scholar
• Park, M. & Moon, R. T. The planar cell-polarity gene stbm regulates cell behavior and cell fate in vertebrate embryos. Nature Cell Biol. 4, 20–25 (2001).
  Article CAS Google Scholar
• Kibar, Z. et al. Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nature Genet. 28, 251–255 (2001).Reports the positional cloning of a classic mouse mutant that is widely used as a model for common neural-tube defects in humans.
  Article CAS PubMed Google Scholar
• Sutherland, D., Samakovlis, C. & Krasnow, M. Branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87, 1091–1102 (1996).
  Article CAS PubMed Google Scholar
• Jarecki, J., Johnson, E. & Krasnow, M. A. Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF. Cell 99, 211–220 (1999).
  Article CAS PubMed Google Scholar
• Mollard, R. & Dziadek, M. A correlation between epithelial proliferation rates, basement membrane component localization patterns, and morphogenetic potential in the embryonic mouse lung. Am. J. Respir. Cell Mol. Biol. 19, 71–82 (1998).
  Article CAS PubMed Google Scholar
• Bluemink, J. G., Van Maurik, P. & Lawson, K. A. Intimate cell contacts at the epithelial/mesenchymal interface in embryonic mouse lung. J. Ultrastruct. Res. 55, 257–270 (1976).
  Article CAS PubMed Google Scholar
• Zent, R. et al. Involvement of laminin binding integrins and laminin-5 in branching morphogenesis of the ureteric bud during kidney development. Dev. Biol. 238, 289–302 (2001).Laminin and its integrin receptors are implicated in ureteric-bud formation in vitro.
  Article CAS PubMed Google Scholar
• Mercurio, A. M., Rabinovitz, I. & Shaw, L. M. The α6β4 integrin and epithelial cell migration. Curr. Opin. Cell Biol. 13, 541–545 (2001).
  Article CAS PubMed Google Scholar
• Trusolino, L., Bertotti, A. & Comoglio, P. M. A signaling adapter function for α6β4 integrin in the control of HGF-dependent invasive growth. Cell 107, 643–654 (2001).The authors show that the α6β4 integrin forms a complex with the HGF receptor, the Met receptor tyrosine kinase, that is required for Met signalling.
  Article CAS PubMed Google Scholar
• Ito, T. et al. Repulsive axon guidance molecule Sema3A inhibits branching morphogenesis of fetal mouse lung. Mech. Dev. 97, 35–45 (2000).
  Article CAS PubMed Google Scholar
• Xian, J. et al. Inadequate lung development and bronchial hyperplasia in mice with a targeted deletion in the Dutt1/Robo1 gene. Proc. Natl Acad. Sci. USA 98, 15062–15066 (2001).This paper implicates Robo1, a receptor for mammalian Slits, in controlling epithelial organization or cell number during lung development. Slits are chemorepellants for axonal growth cones and lymphocytes, but have not yet been implicated in lung development.
  Article CAS PubMed PubMed Central Google Scholar
• Warburton, D. et al. The molecular basis of lung morphogenesis. Mech. Dev. 92, 55–81 (2000).
  Article CAS PubMed Google Scholar
• Risau, W. Mechanisms of angiogenesis. Nature 386, 671–674 (1997).
  Article CAS PubMed Google Scholar
• Drake, C. J. & Fleming, P. A. Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 95, 1671–1679 (2000).
  CAS PubMed Google Scholar
• Drake, C., Brandt, S., Trusk, T. & Little, C. TAL1/SCL is expressed in endothelial progenitor cells/angioblasts and defines a dorsal-to-ventral gradient of vasculogenesis. Dev. Biol. 192, 17–30 (1997).
  Article CAS PubMed Google Scholar
• Cleaver, O. & Krieg, P. A. VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus. Development 125, 3905–3914 (1998).
  CAS PubMed Google Scholar
• Yamaguchi, T. P., Dumont, D. J., Conlon, R. A., Breitman, M. L. & Rossant, J. flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development 118, 489–498 (1993).
  CAS PubMed Google Scholar
• Ferrara, N. Molecular and biological properties of vascular endothelial growth factor. J. Mol. Med. 77, 527–543 (1999).
  Article CAS PubMed Google Scholar
• Carmeliet, P. et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380, 435–439 (1996).
  Article CAS PubMed Google Scholar
• Carmeliet, P. et al. Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Nature Med. 5, 495–502 (1999).
  Article CAS PubMed Google Scholar
• Fong, G. H., Rossant, J., Gertsenstein, M. & Breitman, M. L. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376, 66–70 (1995).
  Article CAS PubMed Google Scholar
• Shalaby, F. et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376, 62–66 (1995).
  Article CAS PubMed Google Scholar
• Dumont, D. J. et al. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282, 946–949 (1998).
  Article CAS PubMed Google Scholar
• Kawasaki, T. et al. A requirement for neuropilin-1 in embryonic vessel formation. Development 126, 4895–4902 (1999).
  CAS PubMed Google Scholar
• Yancopoulos, G. D. et al. Vascular-specific growth factors and blood vessel formation. Nature 407, 242–248 (2000).
  Article CAS PubMed Google Scholar
• Zhong, T. P., Childs, S., Leu, J. P. & Fishman, M. C. Gridlock signalling pathway fashions the first embryonic artery. Nature 414, 216–220 (2001).The authors show that Notch signalling controls vein versus artery identity.
  Article CAS PubMed Google Scholar
• Helbling, P. M., Saulnier, D. M. & Brandli, A. W. The receptor tyrosine kinase EphB4 and ephrin-B ligands restrict angiogenic growth of embryonic veins in Xenopus laevis. Development 127, 269–278 (2000).
  CAS PubMed Google Scholar
• Shin, D. et al. Expression of EphrinB2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev. Biol. 230, 139–150 (2001).The authors found that the arterial marker Ephrin B2 is expressed on capillaries, which indicates that capillaries actually have arterial or venous identity, rather than belonging to a third class of vessel. They also found that Ephrin B2 is expressed in adult arterial smooth muscle, indicating a possible role for Ephrin B2 in the physiology of arterial smooth muscle.
  Article CAS PubMed Google Scholar
• Gale, N. W. et al. Ephrin-B2 selectively marks arterial vessels and neovascularization sites in the adult, with expression in both endothelial and smooth-muscle cells. Dev. Biol. 230, 151–160 (2001).
  Article CAS PubMed Google Scholar
• Takahashi, T. et al. Temporally compartmentalized expression of ephrin-B2 during renal glomerular development. J. Am. Soc. Nephrol. 12, 2673–2682 (2001).
  CAS PubMed Google Scholar
• Childs, S., Chen, J.-N., Garrity, D. M. & Fishman, M. C. Patterning of angiogenesis in the zebrafish embryo. Development 129, 973–982 (2002).This paper describes the assembly of veins in the zebrafish embryo using live imaging, a key advance. The authors also describe a novel mutation, obd , in which the veins are assembled in the wrong places. The obd gene product probably regulates endothelial-cell migration non-cell-autonomously.
  CAS PubMed Google Scholar
• Adams, R. H. et al. The cytoplasmic domain of the ligand EphrinB2 is required for vascular morphogenesis but not cranial neural crest migration. Cell 104, 57–69 (2001).This paper shows that Ephrin B2 ligands signal cell autonomously during vascular morphogenesis, but not during neural-crest migration.
  Article CAS PubMed Google Scholar
• Uemura, T. et al. Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 10, 659–671 (1996).
  Article CAS PubMed Google Scholar
• Tanaka-Matakatsu, M., Uemura, T., Oda, H., Takeichi, M. & Hayashi, S. Cadherin-mediated cell adhesion and motility in Drosophila trachea regulated by the transcription factor Escargot. Development 122, 3697–3705 (1996).
  CAS PubMed Google Scholar
• Bayless, K. J., Salazar, R. & Davis, G. E. RGD-dependent vacuolation and lumen formation observed during endothelial cell morphogenesis in three-dimensional fibrin matrices involves the α(v)β(3) and α(5)β(1) integrins. Am. J. Pathol. 156, 1673–1683 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Maina, F. et al. Coupling Met to specific pathways results in distinct developmental outcomes. Mol. Cell 7, 1293–1306 (2001).Analysis of the effects of different mutants in the Met cytoplasmic domain on its developmental functions. Met orchestrates several distinct responses through the phosphorylation of specific tyrosine residues and the recruitment of different sets of adaptor/signalling molecules.
  Article CAS PubMed Google Scholar
• Pollack, A. L., Runyon, R. B. & Mostov, K. E. Morphogenetic mechanisms of epithelial tubulogenesis: MDCK cell polarity is transiently rearranged without loss of cell–cell contact during scatter factor/hepatocyte growth factor-induced tubulogenesis. Dev. Biol. 204, 64–79 (1998).
  Article CAS PubMed Google Scholar
• O'Brien, L. E. et al. Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nature Cell Biol. 3, 831–838 (2001).The authors show that cell-surface receptors assemble laminin, an extracellular-matrix component, to set the apical–basal polarity for cells in cysts grown in culture. Similar interactions with laminin might define cell polarity in developing tubes in vivo.
  Article CAS PubMed Google Scholar
• Derman, M. P., Chen, J. Y., Spokes, K. C., Songyang, Z. & Cantley, L. G. An 11-amino acid sequence from c-met initiates epithelial chemotaxis via phosphatidylinositol 3-kinase and phospholipase C. J. Biol. Chem. 271, 4251–4255 (1996).
  Article CAS PubMed Google Scholar
• Karihaloo, A., O'Rourke, D. A., Nickel, C., Spokes, K. & Cantley, L. G. Differential MAPK pathways utilized for HGF- and EGF-dependent renal epithelial morphogenesis. J. Biol. Chem. 276, 9166–9173 (2001).
  Article CAS PubMed Google Scholar
• Li, D. & Mrsny, R. J. Oncogenic Raf-1 disrupts epithelial tight junctions via downregulation of occludin. J. Cell Biol. 148, 791–800 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Berrier, A. L., Mastrangelo, A. M., Downward, J., Ginsberg, M. & LaFlamme, S. E. Activated R-ras, Rac1, PI 3-kinase and PKCɛ can each restore cell spreading inhibited by isolated integrin β1 cytoplasmic domains. J. Cell Biol. 151, 1549–1560 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Boccaccio, C. et al. Induction of epithelial tubules by growth factor HGF depends on the STAT pathway. Nature 391, 285–288 (1998).
  Article CAS PubMed Google Scholar
• Beitel, G. J. & Krasnow, M. A. Genetic control of epithelial tube size in the Drosophila tracheal system. Development 127, 3271–3282 (2000).
  CAS PubMed Google Scholar
• LeCouter, J. et al. Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 412, 868–869 (2001).The purification and characterization of a new factor that regulates the development of a subset of endothelial cells. This discovery indicates the existence of several subsets of endothelial cells that might respond to different, perhaps spatially regulated, growth factors.
  Article Google Scholar
• Litingtung, Y., Lei, L., Westphal, H. & Chiang, C. Sonic hedgehog is essential to foregut development. Nature Genet. 20, 58–61 (1998).
  Article CAS PubMed Google Scholar
• Lindahl, P. et al. Alveogenesis failure in PDGF-A-deficient mice is coupled to lack of distal spreading of alveolar smooth muscle cell progenitors during lung development. Development 124, 3943–3953 (1997).
  CAS PubMed Google Scholar
• Cho, N. K. et al. Developmental control of blood cell migration by the Drosophila VEGF pathway. Cell 108, 865–876 (2002).Reports the cloning and expression of Drosophila genes encoding VEGF receptor and VEGF ligands and the failure of blood-cell migration in mutants. The authors speculate about the evolutionary origin of blood vessels and the interdependence of blood cells/vessels and other tubular systems.
  Article CAS PubMed Google Scholar
• Matsumoto, K., Yoshitomi, H., Rossant, J. & Zaret, K. S. Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294, 559–563 (2001).
  Article CAS PubMed Google Scholar
• Lammert, E., Cleaver, O. & Melton, D. Induction of pancreatic differentiation by signals from blood vessels. Science 294, 564–567 (2001).
  Article CAS PubMed Google Scholar