Syk and Slp-76 Mutant Mice Reveal a Cell-Autonomous Hematopoietic Cell Contribution to Vascular Development

Developmental Cell

Volumn 11, Issue 3, 2006, Pages 349-361

  Sebzda, Eric ^a   Hibbard, Chris ^a   Sweeney, Shawn ^a   Abtahian, Farhad ^a,b   Bezman, Natalie ^a,b   Clemens, Gina ^a,b   Maltzman, Jonathan S ^a,b   Cheng, Lan ^a   Liu, Feiyan ^a   Turner, Martin ^c   Tybulewicz, Victor ^d   Koretzky, Gary A ^a,b   Kahn, Mark L ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c BABRAHAM INSTITUTE   (United Kingdom)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

DEVBIO; SIGNALING; STEMCELL

Indexed keywords

GREEN FLUORESCENT PROTEIN; PROTEIN KINASE SYK; PROTEIN SLP 76; SIGNAL TRANSDUCING ADAPTOR PROTEIN; UNCLASSIFIED DRUG;

ADOLESCENT; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CHIMERA; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC TISSUE; MOUSE; MOUSE STRAIN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BIOLOGICAL MARKERS; BLOOD PLATELETS; BLOOD VESSELS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GATA1 TRANSCRIPTION FACTOR; HEMATOPOIETIC SYSTEM; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOID TISSUE; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; NEUTROPHILS; PHOSPHOPROTEINS; PROTEIN-TYROSINE KINASES;

EID: 33747826262     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2006.07.007     Document Type: Article

References (54)

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., et al. Regulation of blood and lymphatic vascular separation by signaling proteins SLP-76 and Syk. Science 299 (2003) 247-251
2. Aicher A., Heeschen C., Mildner-Rihm C., Urbich C., Ihling C., Technau-Ihling K., Zeiher A.M., and Dimmeler S. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat. Med. 9 (2003) 1370-1376
3. Asahara T., Murohara T., Sullivan A., Silver M., van der Zee R., Li T., Witzenbichler B., Schatteman G., and Isner J.M. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275 (1997) 964-967
4. Asahara T., Takahashi T., Masuda H., Kalka C., Chen D., Iwaguro H., Inai Y., Silver M., and Isner J.M. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 18 (1999) 3964-3972
5. Bertolini F., Paul S., Mancuso P., Monestiroli S., Gobbi A., Shaked Y., and Kerbel R.S. Maximum tolerable dose and low-dose metronomic chemotherapy have opposite effects on the mobilization and viability of circulating endothelial progenitor cells. Cancer Res. 63 (2003) 4342-4346
6. Chan A.C., van Oers N.S., Tran A., Turka L., Law C.L., Ryan J.C., Clark E.A., and Weiss A. Differential expression of ZAP-70 and Syk protein tyrosine kinases, and the role of this family of protein tyrosine kinases in TCR signaling. J. Immunol. 152 (1994) 4758-4766
7. Chen H., and Kahn M.L. Reciprocal signaling by integrin and nonintegrin receptors during collagen activation of platelets. Mol. Cell. Biol. 23 (2003) 4764-4777
8. Chen H., Zou Z., Sarratt K.L., Zhou D., Zhang M., Sebzda E., Hammer D.A., and Kahn M.L. In vivo β1 integrin function requires phosphorylation-independent regulation by cytoplasmic tyrosines. Genes Dev. 20 (2006) 927-932
9. Chu D.H., van Oers N.S., Malissen M., Harris J., Elder M., and Weiss A. Pre-T cell receptor signals are responsible for the down-regulation of Syk protein tyrosine kinase expression. J. Immunol. 163 (1999) 2610-2620
10. Clements J.L., Yang B., Ross-Barta S.E., Eliason S.L., Hrstka R.F., Williamson R.A., and Koretzky G.A. Requirement for the leukocyte-specific adapter protein SLP-76 for normal T cell development. Science 281 (1998) 416-419
11. Constien R., Forde A., Liliensiek B., Grone H.J., Nawroth P., Hammerling G., and Arnold B. Characterization of a novel EGFP reporter mouse to monitor Cre recombination as demonstrated by a Tie2 Cre mouse line. Genesis 30 (2001) 36-44
12. Georgiades P., Ogilvy S., Duval H., Licence D.R., Charnock-Jones D.S., Smith S.K., and Print C.G. vavCre transgenic mice: a tool for mutagenesis in hematopoietic and endothelial lineages. Genesis 34 (2002) 251-256
13. Grunewald M., Avraham I., Dor Y., Bachar-Lustig E., Itin A., Yung S., Chimenti S., Landsman L., Abramovitch R., and Keshet E. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124 (2006) 175-189
14. Heissig B., Hattori K., Dias S., Friedrich M., Ferris B., Hackett N.R., Crystal R.G., Besmer P., Lyden D., Moore M.A., et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109 (2002) 625-637
15. Jackman J.K., Motto D.G., Sun Q., Tanemoto M., Turck C.W., Peltz G.A., Koretzky G.A., and Findell P.R. Molecular cloning of SLP-76, a 76-kDa tyrosine phosphoprotein associated with Grb2 in T cells. J. Biol. Chem. 270 (1995) 7029-7032
16. Jin H., Aiyer A., Su J., Borgstrom P., Stupack D., Friedlander M., and Varner J. A homing mechanism for bone marrow-derived progenitor cell recruitment to the neovasculature. J. Clin. Invest. 116 (2006) 652-662
17. Judd B.A., Myung P.S., Obergfell A., Myers E.E., Cheng A.M., Watson S.P., Pear W.S., Allman D., Shattil S.J., and Koretzky G.A. Differential requirement for LAT and SLP-76 in GPVI versus T cell receptor signaling. J. Exp. Med. 195 (2002) 705-717
18. Kennedy M., Firpo M., Choi K., Wall C., Robertson S., Kabrun N., and Keller G. A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature 386 (1997) 488-493
19. Law D.A., Nannizzi-Alaimo L., Ministri K., Hughes P.E., Forsyth J., Turner M., Shattil S.J., Ginsberg M.H., Tybulewicz V.L., and Phillips D.R. Genetic and pharmacological analyses of Syk function in αIIbβ3 signaling in platelets. Blood 93 (1999) 2645-2652
20. Losordo D.W., and Dimmeler S. Therapeutic angiogenesis and vasculogenesis for ischemic disease: part II: cell-base therapies. Circulation 109 (2004) 2692-2697
21. Lyden D., Hattori K., Dias S., Costa C., Blaikie P., Butros L., Chadburn A., Heissig B., Marks W., Witte L., et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat. Med. 7 (2001) 1194-1201
22. Maruyama K., Ii M., Cursiefen C., Jackson D.G., Keino H., Tomita M., Van Rooijen N., Takenaka H., D'Amore P.A., Stein-Streilein J., et al. Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J. Clin. Invest. 115 (2005) 2363-2372
23. McDevitt M.A., Fujiwara Y., Shivdasani R.A., and Orkin S.H. An upstream, DNase I hypersensitive region of the hematopoietic-expressed transcription factor GATA-1 gene confers developmental specificity in transgenic mice. Proc. Natl. Acad. Sci. USA 94 (1997) 7976-7981
24. Migliaccio A.R., Rana R.A., Sanchez M., Lorenzini R., Centurione L., Bianchi L., Vannucchi A.M., Migliaccio G., and Orkin S.H. GATA-1 as a regulator of mast cell differentiation revealed by the phenotype of the GATA-1low mouse mutant. J. Exp. Med. 197 (2003) 281-296
25. Mocsai A., Zhou M., Meng F., Tybulewicz V.L., and Lowell C.A. Syk is required for integrin signaling in neutrophils. Immunity 16 (2002) 547-558
26. Mortensen R.M., Conner D.A., Chao S., Geisterfer-Lowrance A.A., and Seidman J.G. Production of homozygous mutant ES cells with a single targeting construct. Mol. Cell. Biol. 12 (1992) 2391-2395
27. Motoike T., Loughna S., Perens E., Roman B.L., Liao W., Chau T.C., Richardson C.D., Kawate T., Kuno J., Weinstein B.M., et al. Universal GFP reporter for the study of vascular development. Genesis 28 (2000) 75-81
28. Newbrough S.A., Mocsai A., Clemens R.A., Wu J.N., Silverman M.A., Singer A.L., Lowell C.A., and Koretzky G.A. SLP-76 regulates Fcγ receptor and integrin signaling in neutrophils. Immunity 19 (2003) 761-769
29. Obergfell A., Judd B.A., del Pozo M.A., Schwartz M.A., Koretzky G.A., and Shattil S.J. The molecular adapter SLP-76 relays signals from platelet integrin αIIbβ3 to the actin cytoskeleton. J. Biol. Chem. 276 (2001) 5916-5923
30. Papayannopoulou T., and Nakamoto B. Peripheralization of hemopoietic progenitors in primates treated with anti-VLA4 integrin. Proc. Natl. Acad. Sci. USA 90 (1993) 9374-9378
31. Papayannopoulou T., Priestley G.V., and Nakamoto B. Anti-VLA4/VCAM-1-induced mobilization requires cooperative signaling through the kit/mkit ligand pathway. Blood 91 (1998) 2231-2239
32. Pivniouk V., Tsitsikov E., Swinton P., Rathbun G., Alt F.W., and Geha R.S. Impaired viability and profound block in thymocyte development in mice lacking the adaptor protein SLP-76. Cell 94 (1998) 229-238
33. Prevo R., Banerji S., Ferguson D.J., Clasper S., and Jackson D.G. Mouse LYVE-1 is an endocytic receptor for hyaluronan in lymphatic endothelium. J. Biol. Chem. 276 (2001) 19420-19430
34. Rabelink T.J., de Boer H.C., de Koning E.J., and van Zonneveld A.J. Endothelial progenitor cells: more than an inflammatory response?. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 834-838
35. Rafii S., and Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med. 9 (2003) 702-712
36. Rehman J., Li J., Orschell C.M., and March K.L. Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107 (2003) 1164-1169
37. Religa P., Cao R., Bjorndahl M., Zhou Z., Zhu Z., and Cao Y. Presence of bone marrow-derived circulating progenitor endothelial cells in the newly formed lymphatic vessels. Blood 106 (2005) 4184-4190
38. Sabin F. Studies on the origin of blood-vessels and of red blood-corpuscles as seen in the living blastoderm of chicks during the second day of incubation. Contrib. Embryol. Carnegie Inst. 9 (1920) 215-262
39. Salven P., Mustjoki S., Alitalo R., Alitalo K., and Rafii S. VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells. Blood 101 (2003) 168-172
40. Shaked Y., Bertolini F., Man S., Rogers M.S., Cervi D., Foutz T., Rawn K., Voskas D., Dumont D.J., Ben-David Y., et al. Genetic heterogeneity of the vasculogenic phenotype parallels angiogenesis; implications for cellular surrogate marker analysis of antiangiogenesis. Cancer Cell 7 (2005) 101-111
41. Shalaby F., Rossant J., Yamaguchi T.P., Gertsenstein M., Wu X.F., Breitman M.L., and Schuh A.C. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376 (1995) 62-66
42. Shivdasani R.A., and Orkin S.H. Erythropoiesis and globin gene expression in mice lacking the transcription factor NF-E2. Proc. Natl. Acad. Sci. USA 92 (1995) 8690-8694
43. Shivdasani R.A., Fujiwara Y., McDevitt M.A., and Orkin S.H. A lineage-selective knockout establishes the critical role of transcription factor GATA-1 in megakaryocyte growth and platelet development. EMBO J. 16 (1997) 3965-3973
44. Sposi N.M., Zon L.I., Care A., Valtieri M., Testa U., Gabbianelli M., Mariani G., Bottero L., Mather C., Orkin S.H., et al. Cell cycle-dependent initiation and lineage-dependent abrogation of GATA-1 expression in pure differentiating hematopoietic progenitors. Proc. Natl. Acad. Sci. USA 89 (1992) 6353-6357
45. Stadtfeld M., and Graf T. Assessing the role of hematopoietic plasticity for endothelial and hepatocyte development by non-invasive lineage tracing. Development 132 (2005) 203-213
46. Stainier D.Y., Weinstein B.M., Detrich III H.W., Zon L.I., and Fishman M.C. Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages. Development 121 (1995) 3141-3150
47. Suzuki N., Ohneda O., Takahashi S., Higuchi M., Mukai H.Y., Nakahata T., Imagawa S., and Yamamoto M. Erythroid-specific expression of the erythropoietin receptor rescued its null mutant mice from lethality. Blood 100 (2002) 2279-2288
48. 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
49. Visvader J.E., Fujiwara Y., and Orkin S.H. Unsuspected role for the T-cell leukemia protein SCL/tal-1 in vascular development. Genes Dev. 12 (1998) 473-479
50. Werner N., Kosiol S., Schiegl T., Ahlers P., Walenta K., Link A., Bohm M., and Nickenig G. Circulating endothelial progenitor cells and cardiovascular outcomes. N. Engl. J. Med. 353 (2005) 999-1007
51. Whitelaw E., Tsai S.F., Hogben P., and Orkin S.H. Regulated expression of globin chains and the erythroid transcription factor GATA-1 during erythropoiesis in the developing mouse. Mol. Cell. Biol. 10 (1990) 6596-6606
52. 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
53. Yu C., Cantor A.B., Yang H., Browne C., Wells R.A., Fujiwara Y., and Orkin S.H. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J. Exp. Med. 195 (2002) 1387-1395
54. Ziegelhoeffer T., Fernandez B., Kostin S., Heil M., Voswinckel R., Helisch A., and Schaper W. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ. Res. 94 (2004) 230-238