Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts

Nature

Volumn 401, Issue 6754, 1999, Pages 670-677

  Lyden, David ^a   Young, Alison Z ^a   Zagzag, David ^b   Yan, Wei ^a   Gerald, William ^a   O'Reilly, Richard ^a   Bader, Bernhard L ^d   Hynes, Richard O ^c   Zhuang, Yuan ^e   Manova, Katla ^a   Benezra, Robert ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Kaplan Cancer Center   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELIX LOOP HELIX PROTEIN; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 3; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER INHIBITION; CELL DIFFERENTIATION; KNOCKOUT MOUSE; METASTASIS; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR VASCULARIZATION; TUMOR XENOGRAFT;

ANIMALS; ANTIGENS, CD; BRAIN; CELL DIFFERENTIATION; HELIX-LOOP-HELIX MOTIFS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; INTEGRIN ALPHA5; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; NEOPLASM TRANSPLANTATION; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE TISSUE PROTEINS; NEURONS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 0033554723     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/44334     Document Type: Article

References (50)

1. Norton, J. D. et al. Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol. 8, 58-65 (1998).
2. Lassar, A. B., Skapek, S. X. & Novitch, B. Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr. Opin. Cell biol. 6, 788-794 (1994).
3. Ron, D. & Habener, J. F. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as dominant-negative inhibitor of gene transcription. Genes Dev. 6, 439-453 (1992).
4. Treacy, M. N., He, X. & Rosenfeld, M. G. I-POU: a POU-domain protein that inhibits neuron-specific gene activation. Nature 350, 577-584 (1991).
5. Yan, W. et al. High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol. Cell Biol. 17, 7317-7327 (1997).
6. Deed, R. W., Jasiok, M. & Norton, J. D. Lymphoid-specific expression of the Id3 gene in hematopoietic cells. Selective antagonism of E2A basic helix-loop-helix protein associated with Id3-induced differentiation of erythroleukemia cells. J. Biol. Chem. 27, 8278-8286 (1998).
7. Ogata, T. et al. Bone morphogenetic protein 2 transiently enhances expression of a gene, Id (inhibitor of differentiation), encoding a helix-loop-helix molecule in osteoblast-like cells. Proc. Natl Acad. Sci. USA 90, 9219-9222 (1993).
8. Neuman, T. et al. Neuronal expression of regulatory helix-loop-helix factor Id2 gene in mouse. Dev. Biol. 160, 186-195 (1993).
9. Voronova, A. F. & Lee, F. The E2A and tal-1 helix-loop-helix proteins associated in vivo and are modulated by Id proteins during interleukin 6-induced myeloid differentiation. Proc. Natl Acad. Sci. USA 91, 5952-5956 (1994).
10. Heemskerk, M. H. et al. Inhibition of T cells and promotion of natural killer cell development by the dominant negative helix loop helix factor Id3. J. Exp. Med. 186, 1597-1602 (1997).
11. Martinsen, B. J. & Bronner-Fraser, M. Neural crest specification regulated by the helix-loop-helix repressor Id2. Science 281, 988-991 (1998).
12. Katagiri, T. et al. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage [published erratum appears in J. Cell Biol. 128, 713 (1995)]. J. Cell Biol. 127, 1755-1766 (1994).
13. Yokota, Y. et al. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397, 702-706 (1999).
14. Pan, L. et al. Impaired immune responses and B cell proliferation in mice lacking the Id3 gene. Mol. Cell Biol. 19, 5969-5980 (1999).
15. Duncan, M. et al. The gene for the helix-loop-helix protein, Id. is specifically expressed in neural precursors. Dev. Biol. 154, 1-10 (1992).
16. Ellmeier, W. & Weith, A. Expression of the helix-loop-helix gene Id3 during murine embryonic development. Dev. Dyn. 203, 163-173 (1995).
17. Jen, Y., Manova, K. & Benezra, R. Each member of the Id gene family exhibits a unique expression pattern in mouse gastrulation and neurogenesis. Dev. Dyn. 208, 92-106 (1997).
18. Risau, W. Mechanisms of angiogenesis. Nature 386, 671-674 (1997).
19. Lee, J. E. Basic helix-loop-helix genes in neural development. Curr. Opin. Neurobiol. 7, 13-20 (1997).
20. Xuan, S. et al. Winged helix transcription factor BF-1 is essential for the development of the development of the cerebral hemispheres. Neuron 14, 1141-1152 (1995).
21. Price, M. et al. A mouse gene related to Distal-less shows a restricted expression in the developing forebrain. Nature 351, 748-751 (1991).
22. Simeone, A. et al. A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 12, 2735-2747 (1993).
23. Walther, C. & Gruss, P. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449 (1991).
24. Shimamura, K. et al. Longitudinal organization of the anterior neural plate and neural tube. Development 121, 3923-3933 (1995).
25. Bader, B. L. et al. Extensive vasculogenesis, angiogenesis, and organogenesis precede lethality in mice lacking all alpha v integrins. Cell 95, 507-519 (1998).
26. Bain, G. et al. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements [see comments]. Cell 79, 885-892 (1994).
27. Zhuang, Y., Soriano, P. & Weintraub, H. The helix-loop-helix gene E2A is required for B cell formation. Cell 79, 875-884 (1994).
28. Erickson, J. W. & Cline, T. W. Molecular nature of the Drosophila sex determination signal and its link to neurogenesis. Science 251, 1071-1074 (1991).
29. Brooks, P. C. et al. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 85, 683-693 (1996).
30. Perlman, J. M. & Volpe, J. J. Intraventricular hemorrhage in extremely small premature infants. Am. J. Dis. Child. 140, 1122-1124 (1986).
31. Ishibashi, M. et al. Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev. 9, 3136-3148 (1995).
32. Jen, Y., Weintraub, H. & Benezra, R. Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A protein. Genes Dev. 6, 1466-1479 (1992).
33. Melnikova, I. N. & Christy, B. A. Muscle cell differentiation is inhibited by the helix-loop-helix protein Id3. Cell Growth Differ. 7, 1067-1079 (1996).
34. Sherwood, A., Hopp, A. & Smith, J. F. Cellular reactions to subependymal plate haemorrhage in the human neonate. Neuropathol. Appl. Neurobiol. 4, 245-261 (1978).
35. Lindahl, P. et al. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277, 242-245 (1997).
36. Quertermous, E. E. et al. Cloning and characterization of a basic helix-loop-helix protein expressed in early mesoderm and the developing somites. Proc. Natl Acad. Sci. USA 91, 7066-7070 (1994).
37. Brooks, P. C. et al. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 79, 1157-1164 (1994).
38. Zetter, B. R. Angiogenesis and tumor metastasis. Annu. Rev. Med. 49, 407-424 (1998).
39. Desprez, P. Y. et al. A novel pathway for mammary epithelial cell invasion induced by the helix-loop-helix protein Id-1. Mol. Cell Biol. 18, 4577-4588 (1998).
40. O'Reilly, M.S. et al. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88, 277-285 (1997).
41. Boehm, T. et al. Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance [see comments]. Nature 390, 404-407 (1997).
42. Hogan, B. L. et al. Small eyes (Sey): a homozygous lethal mutation on chromosome 2 which affects the differentiation of both lens and nasal placodes in the mouse. J. Embryol. Exp. Morphol. 97, 95-110 (1986).
43. Manova, K. et al. Apoptosis in mouse embryos: elevated levels in pregastrulae and in the distal anterior region of gastrulae of normal and mutant mice. Dev. Dyn. 213, 293-308 (1998).
44. Akazawa, C. et al. A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J. Biol. Chem. 270, 8730-8738 (1995).
45. McCormick, M. B. NeuroD2 and neuroD3: distinct expression patterns and transcriptional activation potentials within the neuroD gene family. Mol. Cell Biol. 16, 5792-5800 (1996).
46. Lee, J. E. et al. Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268, 836-844 (1995).
47. Simonson, M. S., Rooney, A. & Herman, W. H. Expression and differential regulation of Id1, a dominant negative regulator of basic helix-loop-helix transcription factors, in glomerular mesangial cells. Nucleic Acids Res. 21, 5767-5774 (1993).
48. Echelard, Y. et al. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430 (1993).
49. Jen, Y., Manova, K. & Benezra, R. Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev. Dyn. 207, 235-252 (1996).
50. Winnier, G. E., Hargett, L. & Hogan, B. L. The winged helix transcription factor MFHI is required for proliferation and patterning of paraxial mesoderm in the mouse embryo. Genes Dev. 11, 926-940 (1997).