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PMID: 10618416 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The oncogenic LIM-only transcription factor Lmo2 regulates angiogenesis but not vasculogenesis in mice.

Yamada Y, Pannell R, Forster A, Rabbitts TH

Abstract

The LMO2 gene is activated by chromosomal translocations in human T cell acute leukemias, but in mouse embryogenesis, Lmo2 is essential for initiation of yolk sac and definitive hematopoiesis. The LMO2 protein comprises two LIM-zinc-finger-like protein interaction modules and functions by interaction with specific partners in DNA-binding transcription complexes. We have now investigated the role of Lmo2-associated transcription complexes in the formation of the vascular system by following the fate of Lmo2-null embryonic stem (ES) cells in mouse chimeras. Lmo2 is expressed in vascular endothelium, and Lmo2-null ES cells contributed to the capillary network normally until around embryonic day 9. However, after this time, marked disorganization of the vascular system was observed in those chimeric mice that have a high contribution of Lmo2-null ES cells. Moreover, Lmo2-null ES cells do not contribute to endothelial cells of large vessel walls of surviving chimeric mice after embryonic day 10. These results show that Lmo2 is not needed for de novo capillary formation from mesoderm but is necessary for angiogenic remodeling of the existing capillary network into mature vasculature. Thus, Lmo2-mediated transcription complexes not only regulate distinct phases of hematopoiesis but also angiogenesis, presumably by Lmo2 interacting with distinct partners in the different settings.

MeSH Terms
Adaptor Proteins, Signal Transducing Animals Chimera/genetics DNA-Binding Proteins/genetics Embryonic and Fetal Development Endothelium, Vascular/metabolism In Situ Hybridization LIM Domain Proteins Lac Operon Metalloproteins/genetics Mice Neovascularization, Physiologic/genetics Proto-Oncogene Proteins/genetics Recombination, Genetic Stem Cells/metabolism Transcription Factors/genetics beta-Galactosidase
Chemicals
Adaptor Proteins, Signal Transducing DNA-Binding Proteins LIM Domain Proteins Lmo2 protein, mouse Metalloproteins Proto-Oncogene Proteins Transcription Factors beta-Galactosidase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Yamada Y
Medical Research Council Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, United Kingdom.
Pannell R
Forster A
Rabbitts T H
References (38)
38 references, click to expand
  1. The Hox11 gene is essential for cell survival during spleen development.
    Development. 1995 Sep;121(9):2909-15 PMID: 7555717
  2. Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene.
    Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):7075-9 PMID: 7624372
  3. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis.
    Cell. 1996 Aug 9;86(3):353-64 PMID: 8756718
  4. Definitive hematopoiesis is autonomously initiated by the AGM region.
    Cell. 1996 Sep 20;86(6):897-906 PMID: 8808625
  5. The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse.
    EMBO J. 1996 Aug 15;15(16):4123-9 PMID: 8861941
  6. Mechanisms of angiogenesis.
    Nature. 1997 Apr 17;386(6626):671-4 PMID: 9109485
  7. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis.
    Cell. 1997 Jun 13;89(6):981-90 PMID: 9200616
  8. Expression of LIM protein genes Lmo1, Lmo2, and Lmo3 in adult mouse hippocampus and other forebrain regions: differential regulation by seizure activity.
    J Neurosci. 1997 Jul 15;17(14):5549-59 PMID: 9204936
  9. The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins.
    EMBO J. 1997 Jun 2;16(11):3145-57 PMID: 9214632
  10. Unsuspected role for the T-cell leukemia protein SCL/tal-1 in vascular development.
    Genes Dev. 1998 Feb 15;12(4):473-9 PMID: 9472016
  11. A common precursor for hematopoietic and endothelial cells.
    Development. 1998 Feb;125(4):725-32 PMID: 9435292
  12. The T cell leukemia LIM protein Lmo2 is necessary for adult mouse hematopoiesis.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3890-5 PMID: 9520463
  13. The Drosophila LIM-only gene, dLMO, is mutated in Beadex alleles and might represent an evolutionarily conserved function in appendage development.
    Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10637-42 PMID: 9724756
  14. LMO T-cell translocation oncogenes typify genes activated by chromosomal translocations that alter transcription and developmental processes.
    Genes Dev. 1998 Sep 1;12(17):2651-7 PMID: 9732263
  15. Identification and characterization of LMO4, an LMO gene with a novel pattern of expression during embryogenesis.
    Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11257-62 PMID: 9736723
  16. Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny.
    Development. 1998 Nov;125(22):4575-83 PMID: 9778515
  17. A transcription factor party during blood cell differentiation.
    Curr Opin Genet Dev. 1998 Oct;8(5):545-51 PMID: 9794826
  18. Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo.
    Development. 1999 Feb;126(4):793-803 PMID: 9895326
  19. The effect of chromosomal translocations in acute leukemias: the LMO2 paradigm in transcription and development.
    Cancer Res. 1999 Apr 1;59(7 Suppl):1794s-1798s PMID: 10197599
  20. Growth factors acting via endothelial cell-specific receptor tyrosine kinases: VEGFs, angiopoietins, and ephrins in vascular development.
    Genes Dev. 1999 May 1;13(9):1055-66 PMID: 10323857
  21. Detection of specific sequences among DNA fragments separated by gel electrophoresis.
    J Mol Biol. 1975 Nov 5;98(3):503-17 PMID: 1195397
  22. Diffuse intraembryonic hemopoiesis in normal and chimeric avian development.
    Dev Biol. 1981 Nov;88(1):180-91 PMID: 7286444
  23. Diversity and rearrangement of the human T cell rearranging gamma genes: nine germ-line variable genes belonging to two subgroups.
    Cell. 1986 Apr 25;45(2):237-46 PMID: 2938743
  24. Transgenes as probes for active chromosomal domains in mouse development.
    Nature. 1988 Jun 30;333(6176):852-5 PMID: 3386733
  25. Relationship between vasculogenesis, angiogenesis and haemopoiesis during avian ontogeny.
    Development. 1989 Mar;105(3):473-85 PMID: 2612361
  26. The rhombotin family of cysteine-rich LIM-domain oncogenes: distinct members are involved in T-cell translocations to human chromosomes 11p15 and 11p13.
    Proc Natl Acad Sci U S A. 1991 May 15;88(10):4367-71 PMID: 2034676
  27. TTG-2, a new gene encoding a cysteine-rich protein with the LIM motif, is overexpressed in acute T-cell leukaemia with the t(11;14)(p13;q11).
    Oncogene. 1991 Oct;6(10):1887-93 PMID: 1923511
  28. The rhombotin gene family encode related LIM-domain proteins whose differing expression suggests multiple roles in mouse development.
    J Mol Biol. 1992 Aug 5;226(3):747-61 PMID: 1507224
  29. Expression of the TAL1 proto-oncogene in cultured endothelial cells and blood vessels of the spleen.
    Oncogene. 1993 Nov;8(11):3043-6 PMID: 8414504
  30. The oncogenic cysteine-rich LIM domain protein rbtn2 is essential for erythroid development.
    Cell. 1994 Jul 15;78(1):45-57 PMID: 8033210
  31. The LIM protein RBTN2 and the basic helix-loop-helix protein TAL1 are present in a complex in erythroid cells.
    Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8617-21 PMID: 8078932
  32. Specific in vivo association between the bHLH and LIM proteins implicated in human T cell leukemia.
    EMBO J. 1994 Oct 17;13(20):4831-9 PMID: 7957052
  33. The LIM domain: a new structural motif found in zinc-finger-like proteins.
    Trends Genet. 1994 Sep;10(9):315-20 PMID: 7974745
  34. Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL.
    Nature. 1995 Feb 2;373(6513):432-4 PMID: 7830794
  35. Development of hematopoietic stem cell activity in the mouse embryo.
    Immunity. 1994 Jul;1(4):291-301 PMID: 7889417
  36. Endothelial receptor tyrosine kinases involved in angiogenesis.
    J Cell Biol. 1995 May;129(4):895-8 PMID: 7538139
  37. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice.
    Nature. 1995 Jul 6;376(6535):62-6 PMID: 7596435
  38. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages.
    Cell. 1996 Jul 12;86(1):47-57 PMID: 8689686
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2000-01-04
Pages
320-4
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC26661
Subset
IM
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