Growth-limiting role of endothelial cells in endoderm development

Developmental Biology

Volumn 352, Issue 2, 2011, Pages 267-277

  Sand, Fredrik Wolfhagen ^a   Hörnblad, Andreas ^b   Johansson, Jenny K ^a   Lorén, Christina ^b   Edsbagge, Josefina ^c   Ståhlberg, Anders ^a,f   Magenheim, Judith ^d   Ilovich, Ohad ^e   Mishani, Eyal ^e   Dor, Yuval ^d   Ahlgren, Ulf ^b   Semb, Henrik ^a  

^a LUND UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

^c Cellartis AB   (Sweden)

^d HEBREW UNIVERSITY   (Israel)

^e HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^f UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Blood vessel; Endoderm; Mesenchyme; Morphogenesis; Pancreas; Sphingosine 1 phosphate 1 receptor

Indexed keywords

CASPASE 3; SPHINGOSINE 1 PHOSPHATE RECEPTOR; TRANSCRIPTION FACTOR PDX 1; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL HYPERPLASIA; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; ENDOTHELIUM CELL; GENE EXPRESSION; MORPHOGENESIS; MOUSE; NONHUMAN; ORGAN SIZE; ORGANOGENESIS; PANCREAS; PHENOTYPE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STOMACH;

MUS;

EID: 79953028801     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.01.026     Document Type: Article

References (62)

1. Ahlgren U., Jonsson J., Edlund H. The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice. Development 1996, 122:1409-1416.
2. Ahlgren U., Pfaff S.L., Jessell T.M., Edlund T., Edlund H. Independent requirement for ISL1 in formation of pancreatic mesenchyme and islet cells. Nature 1997, 385:257-260.
3. Ahnfelt-Ronne J., Jorgensen M.C., Hald J., Madsen O.D., Serup P., Hecksher-Sorensen J. An improved method for three-dimensional reconstruction of protein expression patterns in intact mouse and chicken embryos and organs. J. Histochem. Cytochem. 2007, 55:925-930.
4. Akeson A.L., Greenberg J.M., Cameron J.E., Thompson F.Y., Brooks S.K., Wiginton D., Whitsett J.A. Temporal and spatial regulation of VEGF-A controls vascular patterning in the embryonic lung. Dev. Biol. 2003, 264:443-455.
5. Alanentalo T., Asayesh A., Morrison H., Loren C.E., Holmberg D., Sharpe J., Ahlgren U. Tomographic molecular imaging and 3D quantification within adult mouse organs. Nat Methods. 2007, 4:31-33.
6. Berg T., Rountree C.B., Lee L., Estrada J., Sala F.G., Choe A., Veltmaat J.M., De Langhe S., Lee R., Tsukamoto H., Crooks G.M., Bellusci S., Wang K.S. Fibroblast growth factor 10 is critical for liver growth during embryogenesis and controls hepatoblast survival via beta-catenin activation. Hepatology 2007, 46:1187-1197.
7. Bhushan A., Itoh N., Kato S., Thiery J.P., Czernichow P., Bellusci S., Scharfmann R. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 2001, 128:5109-5117.
8. Burns R.C., Fairbanks T.J., Sala F., De Langhe S., Mailleux A., Thiery J.P., Dickson C., Itoh N., Warburton D., Anderson K.D., Bellusci S. Requirement for fibroblast growth factor 10 or fibroblast growth factor receptor 2-IIIb signaling for cecal development in mouse. Dev. Biol. 2004, 265:61-74.
9. Chae S.S., Paik J.H., Allende M.L., Proia R.L., Hla T. Regulation of limb development by the sphingosine 1-phosphate receptor S1p1/EDG-1 occurs via the hypoxia/VEGF axis. Dev. Biol. 2004, 268:441-447.
10. Deutsch G., Jung J., Zheng M., Lora J., Zaret K.S. A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 2001, 128:871-881.
11. Dichmann D.S., Miller C.P., Jensen J., Scott Heller R., Serup P. Expression and misexpression of members of the FGF and TGFbeta families of growth factors in the developing mouse pancreas. Dev. Dyn. 2003, 226:663-674.
12. Edsbagge J., Johansson J.K., Esni F., Luo Y., Radice G.L., Semb H. Vascular function and sphingosine-1-phosphate regulate development of the dorsal pancreatic mesenchyme. Development 2005, 132:1085-1092.
13. Elghazi L., Cras-Meneur C., Czernichow P., Scharfmann R. Role for FGFR2IIIb-mediated signals in controlling pancreatic endocrine progenitor cell proliferation. Proc. Natl. Acad. Sci. USA 2002, 99:3884-3889.
14. Esni F., Johansson B.R., Radice G.L., Semb H. Dorsal pancreas agenesis in N-cadherin-deficient mice. Dev. Biol. 2001, 238:202-212.
15. Esni F., Taljedal I.B., Perl A.K., Cremer H., Christofori G., Semb H. Neural cell adhesion molecule (N-CAM) is required for cell type segregation and normal ultrastructure in pancreatic islets. J. Cell Biol. 1999, 144:325-337.
16. Fukuda K., Yasugi S. The molecular mechanisms of stomach development in vertebrates. Dev. Growth Differ. 2005, 47:375-382.
17. Gittes G.K. Developmental biology of the pancreas: a comprehensive review. Dev. Biol. 2009, 326:4-35.
18. Gittes G.K., Galante P.E. A culture system for the study of pancreatic organogenesis. J. Tissue Cult. Meth. 1993, 15:23-27.
19. Golosow N., Grobstein C. Epitheliomesenchymal interaction in pancreatic morphogenesis. Dev. Biol. 1962, 4:242-255.
20. Hebrok M., Kim S.K., Melton D.A. Notochord repression of endodermal Sonic hedgehog permits pancreas development. Genes Dev. 1998, 12:1705-1713.
21. Heinis, M., Simon, M.T., Ilc, K., Mazure, N.M., Pouyssegur, J., Scharfmann, R., Duvillie, B., 2010. Oxygen tension regulates pancreatic beta-cell differentiation through hypoxia-inducible factor 1alpha. Diabetes 59, 662-9.
22. Hori Y., Fukumoto M., Kuroda Y. Enrichment of putative pancreatic progenitor cells from mice by sorting for prominin1 (CD133) and platelet-derived growth factor receptor beta. Stem Cells 2008, 26:2912-2920.
23. Ilovich O., Jacobson O., Aviv Y., Litchi A., Chisin R., Mishani E. Formation of fluorine-18 labeled diaryl ureas-labeled VEGFR-2/PDGFR dual inhibitors as molecular imaging agents for angiogenesis. Bioorg. Med. Chem. 2008, 16:4242-4251.
24. Jacquemin P., Yoshitomi H., Kashima Y., Rousseau G.G., Lemaigre F.P., Zaret K.S. An endothelial-mesenchymal relay pathway regulates early phases of pancreas development. Dev. Biol. 2006, 290:189-199.
25. Kim S.K., Hebrok M., Melton D.A. Notochord to endoderm signaling is required for pancreas development. Development 1997, 124:4243-4252.
26. Kono M., Mi Y., Liu Y., Sasaki T., Allende M.L., Wu Y.P., Yamashita T., Proia R.L. The sphingosine-1-phosphate receptors S1P1, S1P2, and S1P3 function coordinately during embryonic angiogenesis. J. Biol. Chem. 2004, 279:29367-29373.
27. Krapp A., Knofler M., Frutiger S., Hughes G.J., Hagenbuchle O., Wellauer P.K. The p48 DNA-binding subunit of transcription factor PTF1 is a new exocrine pancreas-specific basic helix-loop-helix protein. EMBO J. 1996, 15:4317-4329.
28. Kupperman E., An S., Osborne N., Waldron S., Stainier D.Y. A sphingosine-1-phosphate receptor regulates cell migration during vertebrate heart development. Nature 2000, 406:192-195.
29. Lammert E., Cleaver O., Melton D. Induction of pancreatic differentiation by signals from blood vessels. Science 2001, 294:564-567.
30. LeCouter J., Moritz D.R., Li B., Phillips G.L., Liang X.H., Gerber H.P., Hillan K.J., Ferrara N. Angiogenesis-independent endothelial protection of liver: role of VEGFR-1. Science 2003, 299:890-893.
31. Liu Y., Wada R., Yamashita T., Mi Y., Deng C.X., Hobson J.P., Rosenfeldt H.M., Nava V.E., Chae S.S., Lee M.J., Liu C.H., Hla T., Spiegel S., Proia R.L. Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J. Clin. Invest. 2000, 106:951-961.
32. Martin M., Gallego-Llamas J., Ribes V., Kedinger M., Niederreither K., Chambon P., Dolle P., Gradwohl G. Dorsal pancreas agenesis in retinoic acid-deficient Raldh2 mutant mice. Dev. Biol. 2005, 284:399-411.
33. Matsumoto K., Yoshitomi H., Rossant J., Zaret K.S. Liver organogenesis promoted by endothelial cells prior to vascular function. Science 2001, 294:559-563.
34. 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.
35. Miralles F., Czernichow P., Ozaki K., Itoh N., Scharfmann R. Signaling through fibroblast growth factor receptor 2b plays a key role in the development of the exocrine pancreas. Proc. Natl. Acad. Sci. USA 1999, 96:6267-6272.
36. Nolan T., Hands R.E., Bustin S.A. Quantification of mRNA using real-time RT-PCR. Nat. Protoc. 2006, 1:1559-1582.
37. Nyeng P., Norgaard G.A., Kobberup S., Jensen J. FGF10 signaling controls stomach morphogenesis. Dev. Biol. 2007, 303:295-310.
38. Ohuchi H., Hori Y., Yamasaki M., Harada H., Sekine K., Kato S., Itoh N. FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem. Biophys. Res. Commun. 2000, 277:643-649.
39. Pappu R., Schwab S.R., Cornelissen I., Pereira J.P., Regard J.B., Xu Y., Camerer E., Zheng Y.W., Huang Y., Cyster J.G., Coughlin S.R. Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 2007, 316:295-298.
40. Paris F., Perez G.I., Fuks Z., Haimovitz-Friedman A., Nguyen H., Bose M., Ilagan A., Hunt P.A., Morgan W.F., Tilly J.L., Kolesnick R. Sphingosine 1-phosphate preserves fertility in irradiated female mice without propagating genomic damage in offspring. Nat. Med. 2002, 8:901-902.
41. Revest J.M., Suniara R.K., Kerr K., Owen J.J., Dickson C. Development of the thymus requires signaling through the fibroblast growth factor receptor R2-IIIb. J. Immunol. 2001, 167:1954-1961.
42. Sadahira Y., Ruan F., Hakomori S., Igarashi Y. Sphingosine 1-phosphate, a specific endogenous signaling molecule controlling cell motility and tumor cell invasiveness. Proc. Natl. Acad. Sci. USA 1992, 89:9686-9690.
43. Schwab S.R., Pereira J.P., Matloubian M., Xu Y., Huang Y., Cyster J.G. Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 2005, 309:1735-1739.
44. Schwarz M.A., Zhang F., Gebb S., Starnes V., Warburton D. Endothelial monocyte activating polypeptide II inhibits lung neovascularization and airway epithelial morphogenesis. Mech. Dev. 2000, 95:123-132.
45. 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.
46. Seymour P.A., Freude K.K., Tran M.N., Mayes E.E., Jensen J., Kist R., Scherer G., Sander M. SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc. Natl. Acad. Sci. USA 2007, 104:1865-1870.
47. Shannon J.M., Hyatt B.A. Epithelial-mesenchymal interactions in the developing lung. Annu. Rev. Physiol. 2004, 66:625-645.
48. Spiegel S., Milstien S. Sphingosine 1-phosphate, a key cell signaling molecule. J. Biol. Chem. 2002, 277:25851-25854.
49. Stahlberg A., Elbing K., Andrade-Garda J.M., Sjogreen B., Forootan A., Kubista M. Multiway real-time PCR gene expression profiling in yeast Saccharomyces cerevisiae reveals altered transcriptional response of ADH-genes to glucose stimuli. BMC Genomics 2008, 9:170.
50. Wagner N., Wagner K.D., Theres H., Englert C., Schedl A., Scholz H. Coronary vessel development requires activation of the TrkB neurotrophin receptor by the Wilms' tumor transcription factor Wt1. Genes Dev. 2005, 19:2631-2642.
51. van Tuyl M., Liu J., Wang J., Kuliszewski M., Tibboel D., Post M. Role of oxygen and vascular development in epithelial branching morphogenesis of the developing mouse lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 2005, 288:L167-L178.
52. Warburton D., Schwarz M., Tefft D., Flores-Delgado G., Anderson K.D., Cardoso W.V. The molecular basis of lung morphogenesis. Mech. Dev. 2000, 92:55-81.
53. Venkataraman K., Lee Y.M., Michaud J., Thangada S., Ai Y., Bonkovsky H.L., Parikh N.S., Habrukowich C., Hla T. Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ. Res. 2008, 102:669-676.
54. Wessells N.K., Cohen J.H. Early pancreas organogenesis: morphogenesis, tissue interactions, and mass effects. Dev. Biol. 1967, 15:237-270.
55. West H., Richardson W.D., Fruttiger M. Stabilization of the retinal vascular network by reciprocal feedback between blood vessels and astrocytes. Development 2005, 132:1855-1862.
56. Yatomi Y., Ruan F., Hakomori S., Igarashi Y. Sphingosine-1-phosphate: a platelet-activating sphingolipid released from agonist-stimulated human platelets. Blood 1995, 86:193-202.
57. Yoshitomi H., Zaret K.S. Endothelial cell interactions initiate dorsal pancreas development by selectively inducing the transcription factor Ptf1a. Development 2004, 131:807-817.
58. Zaret K.S. Regulatory phases of early liver development: paradigms of organogenesis. Nat. Rev. Genet. 2002, 3:499-512.
59. Zaret K.S. Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation. Nat. Rev. Genet. 2008, 9:329-340.
60. Zeng X., Wert S.E., Federici R., Peters K.G., Whitsett J.A. VEGF enhances pulmonary vasculogenesis and disrupts lung morphogenesis in vivo. Dev. Dyn. 1998, 211:215-227.
61. Zhang H., Desai N.N., Olivera A., Seki T., Brooker G., Spiegel S. Sphingosine-1-phosphate, a novel lipid, involved in cellular proliferation. J. Cell Biol. 1991, 114:155-167.
62. Zhou Q., Law A.C., Rajagopal J., Anderson W.J., Gray P.A., Melton D.A. A multipotent progenitor domain guides pancreatic organogenesis. Dev. Cell 2007, 13:103-114.