Syk and Zap-70 function redundantly to promote angioblast migration

Developmental Biology

Volumn 340, Issue 1, 2010, Pages 22-29

  Christie, Tara L ^a   Carter, Alyson ^a   Rollins, Evvi Lynn ^a   Childs, Sarah J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Angioblast; Intersegmental vessel; Migration; Syk; Thoracic duct; Vegf; Zap 70; Zebrafish

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE SYK; PROTEIN KINASE ZAP 70; VASCULOTROPIN A;

ANGIOGENESIS; ARTICLE; CELL MIGRATION; DOWN REGULATION; EMBRYO; ENZYME PHOSPHORYLATION; HEMANGIOBLAST; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MESENCHYME CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FUNCTION; THORACIC DUCT; ZEBRA FISH;

DANIO RERIO;

EID: 77649186802     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.01.011     Document Type: Article

References (46)

1. Abtahian F., Guerriero A., Sebzda E., Lu M.M., Zhou R., Mocsai A., Myers E.E., Huang B., Jackson D.G., Ferrari V.A., Tybulewicz V., Lowell C.A., Lepore J.J., Koretzky G.A., and Kahn M.L. Regulation of blood and lymphatic vascular separation by signaling proteins SLP-76 and Syk. Science 299 (2003) 247-251
2. Arpaia E., Shahar M., Dadi H., Cohen A., and Roifman C.M. Defective T cell receptor signaling and CD8+ thymic selection in humans lacking zap-70 kinase. Cell 76 (1994) 947-958
3. Buchner D.A., Su F., Yamaoka J.S., Kamei M., Shavit J.A., Barthel L.K., McGee B., Amigo J.D., Kim S., Hanosh A.W., Jagadeeswaran P., Goldman D., Lawson N.D., Raymond P.A., Weinstein B.M., Ginsburg D., and Lyons S.E. pak2a mutations cause cerebral hemorrhage in redhead zebrafish. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 13996-14001
4. Chan A.C., Kadlecek T.A., Elder M.E., Filipovich A.H., Kuo W.L., Iwashima M., Parslow T.G., and Weiss A. ZAP-70 deficiency in an autosomal recessive form of severe combined immunodeficiency. Science 264 (1994) 1599-1601
5. Cheng A.M., Rowley B., Pao W., Hayday A., Bolen J.B., and Pawson T. Syk tyrosine kinase required for mouse viability and B-cell development. Nature 378 (1995) 303-306
6. Childs S., Chen J.N., Garrity D.M., and Fishman M.C. Patterning of angiogenesis in the zebrafish embryo. Development 129 (2002) 973-982
7. Choi J., Dong L., Ahn J., Dao D., Hammerschmidt M., and Chen J.N. FoxH1 negatively modulates flk1 gene expression and vascular formation in zebrafish. Dev. Biol. 304 (2007) 735-744
8. Cornall R.J., Cheng A.M., Pawson T., and Goodnow C.C. Role of Syk in B-cell development and antigen-receptor signaling. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 1713-1718
9. Covassin L.D., Villefranc J.A., Kacergis M.C., Weinstein B.M., and Lawson N.D. Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 6554-6559
10. Devoto S.H., Melancon E., Eisen J.S., and Westerfield M. Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122 (1996) 3371-3380
11. Elder M.E., Hope T.J., Parslow T.G., Umetsu D.T., Wara D.W., and Cowan M.J. Severe combined immunodeficiency with absence of peripheral blood CD8+ T cells due to ZAP-70 deficiency. Cell. Immunol. 165 (1995) 110-117
12. Elder M.E., Lin D., Clever J., Chan A.C., Hope T.J., Weiss A., and Parslow T.G. Human severe combined immunodeficiency due to a defect in ZAP-70, a T cell tyrosine kinase. Science 264 (1994) 1596-1599
13. Fallah-Arani F., Schweighoffer E., Vanes L., and Tybulewicz V.L. Redundant role for Zap70 in B cell development and activation. Eur. J. Immunol. 38 (2008) 1721-1733
14. Furuhata S., Ando K., Oki M., Aoki K., Ohnishi S., Aoyagi K., Sasaki H., Sakamoto H., Yoshida T., and Ohnami S. Gene expression profiles of endothelial progenitor cells by oligonucleotide microarray analysis. Mol. Cell. Biochem. 298 (2007) 125-138
15. Gelfand E.W., Weinberg K., Mazer B.D., Kadlecek T.A., and Weiss A. Absence of ZAP-70 prevents signaling through the antigen receptor on peripheral blood T cells but not on thymocytes. J. Exp. Med. 182 (1995) 1057-1065
16. Gong Q., White L., Johnson R., White M., Negishi I., Thomas M., and Chan A.C. Restoration of thymocyte development and function in zap-70-/- mice by the Syk protein tyrosine kinase. Immunity 7 (1997) 369-377
17. 2 and Cd3 cross-linking. J. Biol. Chem. 273 (1998) 10771-10776
18. Hogan B.M., Bos F.L., Bussmann J., Witte M., Chi N.C., Duckers H.J., and Schulte-Merker S. Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat. Genet. 41 (2009) 396-398
19. Hong C.C., Peterson Q.P., Hong J.Y., and Peterson R.T. Artery/vein specification is governed by opposing phosphatidylinositol-3 kinase and MAP kinase/ERK signaling. Curr. Biol. 16 (2006) 1366-1372
20. Ichise H., Ichise T., Ohtani O., and Yoshida N. Phospholipase Cgamma2 is necessary for separation of blood and lymphatic vasculature in mice. Development 136 (2009) 191-195
21. Inatome R., Yanagi S., Takano T., and Yamamura H. A critical role for Syk in endothelial cell proliferation and migration. Biochem. Biophys. Res. Commun. 286 (2001) 195-199
22. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., and Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995) 253-310
23. Klemke R.L., Cai S., Giannini A.L., Gallagher P.J., de Lanerolle P., and Cheresh D.A. Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137 (1997) 481-492
24. Kuchler A.M., Gjini E., Peterson-Maduro J., Cancilla B., Wolburg H., and Schulte-Merker S. Development of the zebrafish lymphatic system requires VEGFC signaling. Curr. Biol. 16 (2006) 1244-1248
25. Kwan K.M., Fujimoto E., Grabher C., Mangum B.D., Hardy M.E., Campbell D.S., Parant J.M., Yost H.J., Kanki J.P., and Chien C.B. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236 (2007) 3088-3099
26. Law C.L., Chandran K.A., Sidorenko S.P., and Clark E.A. Phospholipase C-gamma1 interacts with conserved phosphotyrosyl residues in the linker region of Syk and is a substrate for Syk. Mol. Cell. Biol. 16 (1996) 1305-1315
27. Lawson N.D., Mugford J.W., Diamond B.A., and Weinstein B.M. Phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev. 17 (2003) 1346-1351
28. Lawson N.D., and Weinstein B.M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248 (2002) 307-318
29. Lee S., Chen T.T., Barber C.L., Jordan M.C., Murdock J., Desai S., Ferrara N., Nagy A., Roos K.P., and Iruela-Arispe M.L. Autocrine VEGF signaling is required for vascular homeostasis. Cell 130 (2007) 691-703
30. Long Q., Meng A., Wang H., Jessen J.R., Farrell M.J., and Lin S. GATA-1 expression pattern can be recapitulated in living transgenic zebrafish using GFP reporter gene. Development 124 (1997) 4105-4111
31. Marchler-Bauer A B.S. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 32 (2004) 327-331
32. Nasevicius A., Larson J., and Ekker S.C. Distinct requirements for zebrafish angiogenesis revealed by a VEGF-A morphant. Yeast 17 (2000) 294-301
33. Oxtoby E., and Jowett T. Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res. 21 (1993) 1087-1095
34. Parsa K.V., Butchar J.P., Rajaram M.V., Cremer T.J., and Tridandapani S. The tyrosine kinase Syk promotes phagocytosis of Francisella through the activation of Erk. Mol. Immunol. 45 (2008) 3012-3021
35. Roman B.L., Pham V.N., Lawson N.D., Kulik M., Childs S., Lekven A.C., Garrity D.M., Moon R.T., Fishman M.C., Lechleider R.J., and Weinstein B.M. Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 129 (2002) 3009-3019
36. Sebzda E., Hibbard C., Sweeney S., Abtahian F., Bezman N., Clemens G., Maltzman J.S., Cheng L., Liu F., Turner M., Tybulewicz V., Koretzky G.A., and Kahn M.L. Syk and Slp-76 mutant mice reveal a cell-autonomous hematopoietic cell contribution to vascular development. Dev. Cell 11 (2006) 349-361
37. Shan X., Balakir R., Criado G., Wood J.S., Seminario M.C., Madrenas J., and Wange R.L. Zap-70-independent Ca(2+) mobilization and Erk activation in Jurkat T cells in response to T-cell antigen receptor ligation. Mol. Cell. Biol. 21 (2001) 7137-7149
38. Siekmann A.F., and Lawson N.D. Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445 (2007) 781-784
39. Slack E.C., Robinson M.J., Hernanz-Falcon P., Brown G.D., Williams D.L., Schweighoffer E., Tybulewicz V.L., and Reis e Sousa C. Syk-dependent ERK activation regulates IL-2 and IL-10 production by DC stimulated with zymosan. Eur. J. Immunol. 37 (2007) 1600-1612
40. Turner M., Mee P.J., Costello P.S., Williams O., Price A.A., Duddy L.P., Furlong M.T., Geahlen R.L., and Tybulewicz V.L. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature 378 (1995) 298-302
41. Turner M., Schweighoffer E., Colucci F., Di Santo J.P., and Tybulewicz V.L. Tyrosine kinase SYK: essential functions for immunoreceptor signalling. Immunol. Today 21 (2000) 148-154
42. Wigle J.T., Harvey N., Detmar M., Lagutina I., Grosveld G., Gunn M.D., Jackson D.G., and Oliver G. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. Embo. J. 21 (2002) 1505-1513
43. Wigle J.T., and Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 98 (1999) 769-778
44. Williams B.L., Irvin B.J., Sutor S.L., Chini C.C., Yacyshyn E., Bubeck Wardenburg J., Dalton M., Chan A.C., and Abraham R.T. Phosphorylation of Tyr319 in ZAP-70 is required for T-cell antigen receptor-dependent phospholipase C-gamma1 and Ras activation. Embo. J. 18 (1999) 1832-1844
45. Yanagi S., Inatome R., Ding J., Kitaguchi H., Tybulewicz V.L., and Yamamura H. Syk expression in endothelial cells and their morphologic defects in embryonic Syk-deficient mice. Blood 98 (2001) 2869-2871
46. Yaniv K., Isogai S., Castranova D., Dye L., Hitomi J., and Weinstein B.M. Live imaging of lymphatic development in the zebrafish. Nat. Med. 12 (2006) 711-716