Vegfc Regulates Bipotential Precursor Division and Prox1 Expression to Promote Lymphatic Identity in Zebrafish

Cell Reports

Volumn 13, Issue 9, 2015, Pages 1828-1841

  Koltowska, Katarzyna ^a   Lagendijk, Anne Karine ^a   Pichol Thievend, Cathy ^a   Fischer, Johanna C ^c   Francois, Mathias ^a   Ober, Elke A ^b,c   Yap, Alpha S ^a   Hogan, Benjamin M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b University of Copenhagen   (Denmark)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PROSPERO RELATED HOMEOBOX DOMAIN 1; UNCLASSIFIED DRUG; VASCULOTROPIN C; HOMEODOMAIN PROTEIN; PROSPERO-RELATED HOMEOBOX 1 PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CELL DIVISION; CELL FUNCTION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENDOTHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOHISTOCHEMISTRY; LYMPH VESSEL; LYMPHANGIOGENESIS; MOLECULAR DYNAMICS; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; STEM CELL; STRUCTURAL HOMOLOGY; UPREGULATION; ZEBRA FISH; ANGIOGENESIS; ANIMAL; CONFOCAL MICROSCOPY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NONMAMMALIAN EMBRYO; PHYSIOLOGY; REPORTER GENE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIVISION; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; HOMEODOMAIN PROTEINS; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; MICROSCOPY, CONFOCAL; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR C; ZEBRAFISH;

EID: 84947460320     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.10.055     Document Type: Article

References (50)

1. Bos F.L., Caunt M., Peterson-Maduro J., Planas-Paz L., Kowalski J., Karpanen T., van Impel A., Tong R., Ernst J.A., Korving J., et al. CCBE1 is essential for mammalian lymphatic vascular development and enhances the lymphangiogenic effect of vascular endothelial growth factor-C in vivo. Circ. Res. 2011, 109:486-491.
2. Bussmann J., Schulte-Merker S. Rapid BAC selection for tol2-mediated transgenesis in zebrafish. Development 2011, 138:4327-4332.
3. Bussmann J., Bos F.L., Urasaki A., Kawakami K., Duckers H.J., Schulte-Merker S. Arteries provide essential guidance cues for lymphatic endothelial cells in the zebrafish trunk. Development 2010, 137:2653-2657.
4. Ciruna B., Weidinger G., Knaut H., Thisse B., Thisse C., Raz E., Schier A.F. Production of maternal-zygotic mutant zebrafish by germ-line replacement. Proc. Natl. Acad. Sci. USA 2002, 99:14919-14924.
5. Dunworth W.P., Cardona-Costa J., Bozkulak E.C., Kim J.D., Meadows S., Fischer J.C., Wang Y., Cleaver O., Qyang Y., Ober E.A., Jin S.W. Bone morphogenetic protein 2 signaling negatively modulates lymphatic development in vertebrate embryos. Circ. Res. 2014, 114:56-66.
6. François M., Caprini A., Hosking B., Orsenigo F., Wilhelm D., Browne C., Paavonen K., Karnezis T., Shayan R., Downes M., et al. Sox18 induces development of the lymphatic vasculature in mice. Nature 2008, 456:643-647.
7. Geudens I., Gerhardt H. Coordinating cell behaviour during blood vessel formation. Development 2011, 138:4569-4583.
8. Geudens I., Herpers R., Hermans K., Segura I., Ruiz de Almodovar C., Bussmann J., De Smet F., Vandevelde W., Hogan B.M., Siekmann A., et al. Role of delta-like-4/Notch in the formation and wiring of the lymphatic network in zebrafish. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1695-1702.
9. Gilbert S.F. Principles of experimental embryology. Developmental Biology 2000, 49-76. Sinauer Associates. Eighth Edition.
10. Hägerling R., Pollmann C., Andreas M., Schmidt C., Nurmi H., Adams R.H., Alitalo K., Andresen V., Schulte-Merker S., Kiefer F. A novel multistep mechanism for initial lymphangiogenesis in mouse embryos based on ultramicroscopy. EMBO J. 2013, 32:629-644.
11. Hartley J.L., Temple G.F., Brasch M.A. DNA cloning using in vitro site-specific recombination. Genome Res. 2000, 10:1788-1795.
12. Helker C.S., Schuermann A., Karpanen T., Zeuschner D., Belting H.G., Affolter M., Schulte-Merker S., Herzog W. The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment. Development 2013, 140:2776-2786.
13. Herpers R., van de Kamp E., Duckers H.J., Schulte-Merker S. Redundant roles for sox7 and sox18 in arteriovenous specification in zebrafish. Circ. Res. 2008, 102:12-15.
14. Hirata J., Nakagoshi H., Nabeshima Y., Matsuzaki F. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 1995, 377:627-630.
15. Hogan B.M., Bos F.L., Bussmann J., Witte M., Chi N.C., Duckers H.J., Schulte-Merker S. Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat. Genet. 2009, 41:396-398.
16. Hogan B.M., Herpers R., Witte M., Heloterä H., Alitalo K., Duckers H.J., Schulte-Merker S. Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries. Development 2009, 136:4001-4009.
17. Hong Y.K., Harvey N., Noh Y.H., Schacht V., Hirakawa S., Detmar M., Oliver G. Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Dev. Dyn. 2002, 225:351-357.
18. Isogai S., Hitomi J., Yaniv K., Weinstein B.M. Zebrafish as a new animal model to study lymphangiogenesis. Anat. Sci. Int. 2009, 84:102-111.
19. Jeltsch M., Jha S.K., Tvorogov D., Anisimov A., Leppänen V.M., Holopainen T., Kivelä R., Ortega S., Kärpanen T., Alitalo K. CCBE1 enhances lymphangiogenesis via A disintegrin and metalloprotease with thrombospondin motifs-3-mediated vascular endothelial growth factor-C activation. Circulation 2014, 129:1962-1971.
20. Johnson N.C., Dillard M.E., Baluk P., McDonald D.M., Harvey N.L., Frase S.L., Oliver G. Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev. 2008, 22:3282-3291.
21. Karkkainen M.J., Haiko P., Sainio K., Partanen J., Taipale J., Petrova T.V., Jeltsch M., Jackson D.G., Talikka M., Rauvala H., et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 2004, 5:74-80.
22. Kartopawiro J., Bower N.I., Karnezis T., Kazenwadel J., Betterman K.L., Lesieur E., Koltowska K., Astin J., Crosier P., Vermeren S., et al. Arap3 is dysregulated in a mouse model of hypotrichosis-lymphedema-telangiectasia and regulates lymphatic vascular development. Hum. Mol. Genet. 2014, 23:1286-1297.
23. Kim H., Nguyen V.P., Petrova T.V., Cruz M., Alitalo K., Dumont D.J. Embryonic vascular endothelial cells are malleable to reprogramming via Prox1 to a lymphatic gene signature. BMC Dev. Biol. 2010, 10:72.
24. Klotz L., Norman S., Vieira J.M., Masters M., Rohling M., Dubé K.N., Bollini S., Matsuzaki F., Carr C.A., Riley P.R. Cardiac lymphatics are heterogeneous in origin and respond to injury. Nature 2015, 522:62-67.
25. Kok F.O., Shin M., Ni C.W., Gupta A., Grosse A.S., van Impel A., Kirchmaier B.C., Peterson-Maduro J., Kourkoulis G., Male I., et al. Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. Dev. Cell 2015, 32:97-108.
26. Koltowska K., Betterman K.L., Harvey N.L., Hogan B.M. Getting out and about: the emergence and morphogenesis of the vertebrate lymphatic vasculature. Development 2013, 140:1857-1870.
27. Koltowska K., Paterson S., Bower N.I., Baillie G.J., Lagendijk A.K., Astin J.W., Chen H., Francois M., Crosier P.S., Taft R.J., et al. mafba is a downstream transcriptional effector of Vegfc signaling essential for embryonic lymphangiogenesis in zebrafish. Genes Dev. 2015, 29:1618-1630.
28. Lawson N.D., Weinstein B.M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 2002, 248:307-318.
29. Le Guen L., Karpanen T., Schulte D., Harris N.C., Koltowska K., Roukens G., Bower N.I., van Impel A., Stacker S.A., Achen M.G., et al. Ccbe1 regulates Vegfc-mediated induction of Vegfr3 signaling during embryonic lymphangiogenesis. Development 2014, 141:1239-1249.
30. Mahadevan A., Welsh I.C., Sivakumar A., Gludish D.W., Shilvock A.R., Noden D.M., Huss D., Lansford R., Kurpios N.A. The left-right Pitx2 pathway drives organ-specific arterial and lymphatic development in the intestine. Dev. Cell 2014, 31:690-706.
31. Martinez-Corral I., Ulvmar M.H., Stanczuk L., Tatin F., Kizhatil K., John S.W., Alitalo K., Ortega S., Makinen T. Nonvenous origin of dermal lymphatic vasculature. Circ. Res. 2015, 116:1649-1654.
32. Nicenboim J., Malkinson G., Lupo T., Asaf L., Sela Y., Mayseless O., Gibbs-Bar L., Senderovich N., Hashimshony T., Shin M., et al. Lymphatic vessels arise from specialized angioblasts within a venous niche. Nature 2015, 522:56-61.
33. Okuda K.S., Astin J.W., Misa J.P., Flores M.V., Crosier K.E., Crosier P.S. lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish. Development 2012, 139:2381-2391.
34. Pistocchi A., Bartesaghi S., Cotelli F., Del Giacco L. Identification and expression pattern of zebrafish prox2 during embryonic development. Dev. Dyn. 2008, 237:3916-3920.
35. Pistocchi A., Gaudenzi G., Carra S., Bresciani E., Del Giacco L., Cotelli F. Crucial role of zebrafish prox1 in hypothalamic catecholaminergic neurons development. BMC Dev. Biol. 2008, 8:27.
36. Sabin F.R. On the origin of the lymphatic system from the veins and the development of the lymph hearts and thoracic duct in the pig. Am. J. Anat. 1902, 1:367-389.
37. Sauteur L., Krudewig A., Herwig L., Ehrenfeuchter N., Lenard A., Affolter M., Belting H.G. Cdh5/VE-cadherin promotes endothelial cell interface elongation via cortical actin polymerization during angiogenic sprouting. Cell Rep. 2014, 9:504-513.
38. Srinivasan R.S., Oliver G. Prox1 dosage controls the number of lymphatic endothelial cell progenitors and the formation of the lymphovenous valves. Genes Dev. 2011, 25:2187-2197.
39. Srinivasan R.S., Dillard M.E., Lagutin O.V., Lin F.J., Tsai S., Tsai M.J., Samokhvalov I.M., Oliver G. Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev. 2007, 21:2422-2432.
40. Srinivasan R.S., Geng X., Yang Y., Wang Y., Mukatira S., Studer M., Porto M.P., Lagutin O., Oliver G. The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes Dev. 2010, 24:696-707.
41. Srinivasan R.S., Escobedo N., Yang Y., Interiano A., Dillard M.E., Finkelstein D., Mukatira S., Gil H.J., Nurmi H., Alitalo K., Oliver G. The Prox1-Vegfr3 feedback loop maintains the identity and the number of lymphatic endothelial cell progenitors. Genes Dev. 2014, 28:2175-2187.
42. Stanczuk L., Martinez-Corral I., Ulvmar M.H., Zhang Y., Laviña B., Fruttiger M., Adams R.H., Saur D., Betsholtz C., Ortega S., et al. cKit lineage hemogenic endothelium-derived cells contribute to mesenteric lymphatic vessels. Cell Rep. 2015, Published online March 10, 2015. 10.1016/j.celrep.2015.02.026.
43. Tao S., Witte M., Bryson-Richardson R.J., Currie P.D., Hogan B.M., Schulte-Merker S. Zebrafish prox1b mutants develop a lymphatic vasculature, and prox1b does not specifically mark lymphatic endothelial cells. PLoS ONE 2011, 6:e28934.
44. van Impel A., Zhao Z., Hermkens D.M., Roukens M.G., Fischer J.C., Peterson-Maduro J., Duckers H., Ober E.A., Ingham P.W., Schulte-Merker S. Divergence of zebrafish and mouse lymphatic cell fate specification pathways. Development 2014, 141:1228-1238.
45. Villefranc J.A., Nicoli S., Bentley K., Jeltsch M., Zarkada G., Moore J.C., Gerhardt H., Alitalo K., Lawson N.D. A truncation allele in vascular endothelial growth factor c reveals distinct modes of signaling during lymphatic and vascular development. Development 2013, 140:1497-1506.
46. Wigle J.T., Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999, 98:769-778.
47. Wigle J.T., Harvey N., Detmar M., Lagutina I., Grosveld G., Gunn M.D., Jackson D.G., Oliver G. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J. 2002, 21:1505-1513.
48. Yang Y., García-Verdugo J.M., Soriano-Navarro M., Srinivasan R.S., Scallan J.P., Singh M.K., Epstein J.A., Oliver G. Lymphatic endothelial progenitors bud from the cardinal vein and intersomitic vessels in mammalian embryos. Blood 2012, 120:2340-2348.
49. Yaniv K., Isogai S., Castranova D., Dye L., Hitomi J., Weinstein B.M. Live imaging of lymphatic development in the zebrafish. Nat. Med. 2006, 12:711-716.
50. Yu F., Kuo C.T., Jan Y.N. Drosophila neuroblast asymmetric cell division: recent advances and implications for stem cell biology. Neuron 2006, 51:13-20.