SCL interacts with VEGF to suppress apoptosis at the onset of hematopoiesis

Development

Volumn 131, Issue 3, 2004, Pages 693-702

  Martin, Richard ^a,b   Lahlil, Rachid ^a   Damert, Annette ^c,f   Miquerol, Lucile ^c,g   Nagy, Andras ^c   Keller, Gordon ^d   Hoang, Trang ^a,b,e,h  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e UNIVERSITÉ DE MONTRÉAL   (Canada)

^f CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^g AIX MARSEILLE UNIVERSITÉ   (France)

^h INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

Author keywords

ES cell differentiation; Hematopoiesis; Mouse; Primitive erythropoiesis; SCL; TAL1; VEGF

Indexed keywords

DNA BINDING PROTEIN; HELIX LOOP HELIX PROTEIN; ONCOPROTEIN; T CELL ACUTE LYMPHOCYTIC LEUKEMIA 1 PROTEIN; T-CELL ACUTE LYMPHOCYTIC LEUKEMIA 1 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SCL; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ALLELE; ANIMAL; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CLONE; CELL MATURATION; CELL MIGRATION; CELL MOTION; CELL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; EMBRYO DEVELOPMENT; ERYTHROCYTE; ERYTHROID CELL; ERYTHROID PRECURSOR CELL; GENE FUNCTION; GENETICS; HEMATOLOGIC DISEASE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IN VIVO STUDY; LETHAL GENE; METABOLISM; MOUSE; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; YOLK SAC;

ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL MOVEMENT; DNA-BINDING PROTEINS; ERYTHROCYTES; ERYTHROID CELLS; GENES, LETHAL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; MICE; PROTO-ONCOGENE PROTEINS; TRANSCRIPTION FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ANIMALIA; SIGANUS;

EID: 1242285120     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00968     Document Type: Article

References (52)

1. Aplan, P. D., Jones, C. A., Chervinsky, D. S., Zhao, X., Ellsworth, M., Wu, C., McGuire, E. A. and Gross, K. W. (1997). An scl gene product lacking the transactivation domain induces bony abnormalities and cooperates with LMO1 to generate T-cell malignancies in transgenic mice. EMBO J. 16, 2408-2419.
2. Begley, C. G., Aplan, P. D., Denning, S. M., Haynes, B. F., Waldmann, T. A. and Kirsch, I. R. (1989). The gene SCL is expressed during early hematopoiesis and encodes a differentiation-related DNA-binding motif. Proc. Natl. Acad. Sci. USA 86, 10128-10132.
3. Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., Fahrig, M., Vandenhoeck, A., Harpal, K., Eberhardt, C., Declercq, C., Pawling, J., Moons, L., Collen, D., Risau, W. and Nagy, A. (1996), Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380, 435-439.
4. Chen, Q., Cheng, J. T., Tasi, L. H., Schneider, N., Buchanan, G., Carroll, A., Crist, W., Ozanne, B., Siciliano, M. J. and Baer, R. (1990). The tal gene undergoes chromosome translocation in T cell leukemia and potentially encodes a helix-loop-helix protein. EMBO J. 9, 415-424.
5. Cho, N. K., Keyes, L., Johnson, E., Heller, J., Ryner, L., Karim, F. and Krasnow, M. A. (2002). Developmental control of blood cell migration by the Drosophila VEGF pathway. Cell 108, 865-876.
6. Choi, K., Kennedy, M., Kazarov, A., Papadimitriou, J. C. and Keller, G. (1998). A common precursor for hematopoietic and endothelial cells. Development 125, 725-732.
7. Chung, Y. S., Zhang, W. J., Arentson, E., Kingsley, P. D., Palis, J. and Choi, K. (2002). Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression. Development 129, 5511-5520.
8. Damert, A., Miquerol, L., Gertsenstein, M., Risau, W. and Nagy, A. (2002). Insufficient VEGFA activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation. Development 129, 1881-1892.
9. Davis, R. L., Weintraub, H. and Lassar, A. B. (1987). Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51, 987-1000.
10. Drake, C. J. and Fleming, P. A. (2000). Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 95, 1671-1679.
11. Elefanty, A. G., Begley, C. G., Hartley, L., Papaevangeliou, B. and Robb, L. (1999). SCL expression in the mouse embryo detected with a targeted lacZ reporter gene demonstrates its localization to hematopoietic, vascular, and neural tissues. Blood 94, 3754-3763.
12. Ema, M., Faloon, P., Zhang, W. J., Hirashima, M., Reid, T., Stanford, W. L., Orkin, S., Choi, K. and Rossant, J. (2003). Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse. Genes Dev. 17, 380-393.
13. Faloon, P., Arentson, E., Kazarov, A., Deng, C. X., Porcher, C., Orkin, S. and Choi, K. (2000). Basic fibroblast growth factor positively regulates hematopoietic development. Development 127, 1931-1941.
14. Ferrara, N. and Henzel, W. J. (1989). Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem. Biophys. Res. Commun. 161, 851-858.
15. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K. S., Powell-Braxton, L., Hillan, K. J. and Moore, M. W. (1996). Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439-442.
16. Ferrara, N., Gerber, H. P. and LeCouter, J. (2003). The biology of VEGF and its receptors. Nat. Med. 9, 669-676.
17. Finger, L. R., Kagan, J., Christopher, G., Kurtzberg, J., Hershfield, M. S., Nowell, P. C. and Croce, C. M. (1989). Involvement of the TCL5 gene on human chromosome 1 in T-cell leukemia and melanoma. Proc. Natl. Acad. Sci. USA 86, 5039-5043.
18. Fong, G. H., Klingensmith, J., Wood, C. R., Rossant, J. and Breitman, M. L. (1996). Regulation of flt-1 expression during mouse embryogenesis suggests a role in the establishment of vascular endothelium. Dev. Dyn. 207, 1-10.
19. Gerber, H. P., Malik, A. K., Solar, G. P., Sherman, D., Liang, X. H., Meng, G., Hong, K., Marsters, J. C. and Ferrara, N. (2002). VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 417, 954-958.
20. Gering, M., Rodaway, A. R., Gottgens, B., Patient, R. K. and Green, A. R. (1998). The SCL gene specifies haemangioblast development from early mesoderm. EMBO J. 17, 4029-4045.
21. Gospodarowicz, D., Abraham, J. A. and Schilling, J. (1989). Isolation and characterization of a vascular endothelial cell mitogen produced by pituitary-derived folliculo stellate cells. Proc. Natl. Acad. Sci. USA 86, 7311-7315.
22. Herblot, S., Steff, A. M., Hugo, P., Aplan, P. D. and Hoang, T. (2000). SCL and LMO1 alter thymocyte differentiation: inhibition of E2A-HEB function and pre-T alpha chain expression. Nat. Immunol. 1, 138-144.
23. Hidaka, M., Stanford, W. L. and Bernstein, A. (1999). Conditional requirement for the Flk-1 receptor in the in vitro generation of early hematopoietic cells. Proc. Natl. Acad. Sci. USA 96, 7370-7375.
24. Hiratsuka, S., Minowa, O., Kano, J., Noda, T. and Shibuya, M. (1998). Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc. Natl. Acad. Sci. USA 95, 9349-9354.
25. Hoang, T., Paradis, E., Brady, G., Billia, F., Nakabara, K., Iscove, N. N. and Kirsch, I. R. (1996). Opposing effects of the basic helix-loop-helix transcription factor SCL on erythroid and monocytic differentiation. Blood 87, 102-111.
26. Kabrun, N., Buhring, H. J., Choi, K., Ullrich, A., Risau, W. and Keller, G. (1997). Flk-1 expression defines a population of early embryonic hematopoietic precursors. Development 124, 2039-2048.
27. Keller, G., Kennedy, M., Papayannopoulou, T. and Wiles, M. V. (1993). Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol. Cell. Biol. 13, 473-486.
28. Kennedy, M., Firpo, M., Choi, K., Wall, C., Robertson, S., Kabrun, N. and Keller, G. (1997). A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature 386, 488-493.
29. Krosl, G., He, G., Lefrancois, M., Charron, F., Romeo, P. H., Jolicoeur, P., Kirsch, I. R., Nemer, M. and Hoang, T. (1998). Transcription factor SCL is required for c-kit expression and c-Kit function in hemopoietic cells. J. Exp. Med. 188, 439-450.,
30. Liao, W., Bisgrove, B. W., Sawyer, H., Hug, B., Bell, B., Peters, K., Grunwald, D. J. and Stainier, D. Y. (1997). The zebrafish gene cloche acts upstream of a flk-1 homologue to regulate endothelial cell differentiation. Development 124, 381-389.
31. Liao, E. C., Paw, B. H., Oates, A. C., Pratt, S. J., Postlethwait, J. H. and Zon, L. I. (1998). SCL/Tal-1 transcription factor acts downstream of cloche to specify hematopoietic and vascular progenitors in zebrafish. Genes Dev. 12, 621-626.
32. Matthews, W., Jordan, C. T., Gavin, M., Jenkins, N. A., Copeland N. G. and Lemischka, I. R. (1991). A receptor tyrosine kinase cDNA isolated from a population of enriched primitive hematopoietic cells and exhibiting close genetic linkage to c-kit. Proc. Natl. Acad. Sci. USA 88, 9026-9030.
33. Mead, P. E., Kelley, C. M., Hahn, P. S., Piedad, O. and Zon, L. I. (1998). SCL specifies hematopoietic mesoderm in Xenopus embryos. Development 125, 2611-2620.
34. Mead, P. E., Deconinck, A. E., Huber, T. L., Orkin, S. H. and Zon, L. I. (2001). Primitive erythropoiesis in the Xenopus embryo: the synergistic role of LMO-2, SCL and GATA-binding proteins. Development 128, 2301-2308.
35. Millauer, B., Wizigmann-Voos, S., Schnurch, H., Martinez, R., Moller, N. P., Risau, W. and Ullrich, A. (1993). High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72, 835-846.
36. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. and Roder, J. C. (1993). Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90, 8424-8428.
37. Palis, J., Robertson, S., Kennedy, M., Wall, C. and Keller, G. (1999). Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 126, 5073-5084.
38. Porcher, C., Swat, W., Rockwell, K., Fujiwara, Y., Alt, F. W. and Orkin, S. H. (1996). The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 86, 47-57.
39. Robb, L., Lyons, I., Li, R., Hartley, L., Kontgen, F., Harvey, R. P., Metcalf, D. and Begley, C. G. (1995). Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc. Natl. Acad. Sci. USA 92, 7075-7079.
40. Robb, L., Elwood, N. J., Elefanty, A. G., Kontgen, F., Li, R., Barnett, L. D. and Begley, C. G. (1996). The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J. 15, 4123-4129.
41. Robertson, E., Bradley, A., Kuehn, M. and Evans, M. (1986). Germ-line transmission of genes introduced into cultured pluripotential cells by retroviral vector. Nature 323, 445-448.
42. Robertson, S. M., Kennedy, M., Shannon, J. M. and Keller, G. (2000). A transitional stage in the commitment of mesoderm to hematopoiesis requiring the transcription factor SCL/tal-1. Development 127, 2447-2459.
43. Rubin, H. (1998). Telomerase and cellular lifespan: ending the debate? Nat. Biotechnol. 16, 396-397.
44. Sauvageau, G., Lansdorp, P. M., Eaves, C. J., Hogge, D. E., Dragowska, W. H., Reid, D. S., Largman, C., Lawrence, H. J. and Humphries, R. K. (1994). Differential expression of homeobox genes in functionally distinct CD34+ subpopulations of human bone marrow cells. Proc. Natl. Acad. Sci. USA 91, 12223-12227.
45. Schuh, A. C., Faloon, P., Hu, Q. L., Bhimani, M. and Choi, K. (1999). In vitro hematopoietic and endothelial potential of flk-1(-/-) embryonic stem cells and embryos. Proc. Natl. Acad. Sci. USA 96, 2159-2164.
46. Shalaby, F., Rossant, J., Yamaguchi, T. P., Gertsenstein, M., Wu, X. F., Breitman, M. L. and Schuh, A. C. (1995). Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376, 62-66.
47. Shalaby, F., Ho, J., Stanford, W. L., Fischer, K. D., Schuh, A. C., Schwartz, L., Bernstein, A. and Rossant, J. (1997). A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 89, 981-990.
48. Sherr, C. J. and DePinho, R. A. (2000). Cellular senescence: mitotic clock or culture shock? Cell 102, 407-410.
49. Shibuya, M., Yamaguchi, S., Yamane, A., Ikeda, T., Tojo, A., Matsushime, H. and Sato, M. (1990). Nucleotide sequence and expression of a novel human receptor-type tyrosine kinase gene (flt) closely related to the fms family. Oncogene 5, 519-524.
50. Shivdasani, R. A., Mayer, E. L. and Orkin, S. H. (1995). Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 373, 432-434.
51. Visvader, J. E., Fujiwara, Y. and Orkin, S. H. (1998). Unsuspected role for the T-cell leukemia protein SCL/tal-1 in vascular development. Genes Dev. 12, 473-479.
52. Yamaguchi, T. P., Dumont, D. J., Conlon, R. A., Breitman, M. L. and Rossant, J. (1993). flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development 118, 489-498.