Id2 Mediates Tumor Initiation, Proliferation, and Angiogenesis in Rb Mutant Mice

REFERENCES

• Aoki, K., Y. Tamai, S. Horiike, M. Oshima, and M. M. Taketo. 2003. Colonic polyposis caused by mTOR-mediated chromosomal instability in Apc+/Delta716 Cdx2+/− compound mutant mice. Nat. Genet. 35:323–330.
   PubMed Web of Science ®Google Scholar
• Backman, U., A. Svensson, and R. Christofferson. 2002. Importance of vascular endothelial growth factor A in the progression of experimental neuroblastoma. Angiogenesis 5:267–274.
   PubMedGoogle Scholar
• Bardos, J. I., N. M. Chau, and M. Ashcroft. 2004. Growth factor-mediated induction of HDM2 positively regulates hypoxia-inducible factor 1α expression. Mol. Cell. Biol. 24:2905–2914.
   PubMed Web of Science ®Google Scholar
• Baudino, T. A., C. McKay, H. Pendeville-Samain, J. A. Nilsson, K. H. Maclean, E. L. White, A. C. Davis, J. N. Ihle, and J. L. Cleveland. 2002. c-Myc is essential for vasculogenesis and angiogenesis during development and tumor progression. Genes Dev. 16:2530–2543.
   PubMed Web of Science ®Google Scholar
• Bergers, G., and L. E. Benjamin. 2003. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 3:401–410.
   PubMed Web of Science ®Google Scholar
• Brugarolas, J. B., F. Vazquez, A. Reddy, W. R. Sellers, and W. G. Kaelin, Jr. 2003. TSC2 regulates VEGF through mTOR-dependent and -independent pathways. Cancer Cell 4:147–158.
   PubMed Web of Science ®Google Scholar
• Chappell, S. A., T. Walsh, R. A. Walker, and J. A. Shaw. 1997. Loss of heterozygosity at the mannose 6-phosphate insulin-like growth factor 2 receptor gene correlates with poor differentiation in early breast carcinomas. Br. J. Cancer 76:1558–1561.
   PubMedGoogle Scholar
• Chen, D., I. Livne-bar, J. L. Vanderluit, R. S. Slack, M. Agochiya, and R. Bremner. 2004. Cell-specific effects of RB or RB/p107 loss on retinal development implicate an intrinsically death-resistant cell-of-origin in retinoblastoma. Cancer Cell 5:539–551.
   PubMedGoogle Scholar
• Eggert, A., N. Ikegaki, J. Kwiatkowski, H. Zhao, G. M. Brodeur, and B. P. Himelstein. 2000. High-level expression of angiogenic factors is associated with advanced tumor stage in human neuroblastomas. Clin. Cancer Res. 6:1900–1908.
   PubMed Web of Science ®Google Scholar
• Farah, M. H., J. M. Olson, H. B. Sucic, R. I. Hume, S. J. Tapscott, and D. L. Turner. 2000. Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 127:693–702.
   PubMed Web of Science ®Google Scholar
• Fernandez, P. C., S. R. Frank, L. Wang, M. Schroeder, S. Liu, J. Greene, A. Cocito, and B. Amati. 2003. Genomic targets of the human c-Myc protein. Genes Dev. 17:1115–1129.
   PubMed Web of Science ®Google Scholar
• Ferrara, N. 2002. VEGF and the quest for tumour angiogenesis factors. Nat. Rev. Cancer 2:795–803.
   PubMed Web of Science ®Google Scholar
• Fukuma, M., H. Okita, J. Hata, and A. Umezawa. 2003. Upregulation of Id2 an oncogenic helix-loop-helix protein, is mediated by the chimeric EWS/ets protein in Ewing sarcoma. Oncogene 22:1–9.
   PubMed Web of Science ®Google Scholar
• Haggerty, T. J., K. I. Zeller, R. C. Osthus, D. R. Wonsey, and C. V. Dang. 2003. A strategy for identifying transcription factor binding sites reveals two classes of genomic c-Myc target sites. Proc. Natl. Acad. Sci. USA 100:5313–5318.
   PubMedGoogle Scholar
• Hu, N., A. Gutsmann, D. C. Herbert, A. Bradley, W. H. Lee, and E. Y. Lee. 1994. Heterozygous Rb-1 delta 20/+ mice are predisposed to tumors of the pituitary gland with a nearly complete penetrance. Oncogene 9:1021–1027.
   PubMedGoogle Scholar
• Iakova, P., S. S. Awad, and N. A. Timchenko. 2003. Aging reduces proliferative capacities of liver by switching pathways of C/EBPalpha growth arrest. Cell 113:495–506.
   PubMed Web of Science ®Google Scholar
• Iavarone, A., P. Garg, A. Lasorella, J. Hsu, and M. A. Israel. 1994. The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev. 8:1270–1284.
   PubMedGoogle Scholar
• Iavarone, A., E. R. King, X. M. Dai, G. Leone, E. R. Stanley, and A. Lasorella. 2004. Retinoblastoma promotes definitive erythropoiesis by repressing Id2 in fetal liver macrophages. Nature 432:1040–1045.
   PubMed Web of Science ®Google Scholar
• Inoue, M., J. H. Hager, N. Ferrara, H. P. Gerber, and D. Hanahan. 2002. VEGF-A has a critical, nonredundant role in angiogenic switching and pancreatic beta cell carcinogenesis. Cancer Cell 1:193–202.
   PubMed Web of Science ®Google Scholar
• Jacks, T., A. Fazeli, E. M. Schmitt, R. T. Bronson, M. A. Goodell, and R. A. Weinberg. 1992. Effects of an Rb mutation in the mouse. Nature 359:295–300.
   PubMed Web of Science ®Google Scholar
• Jen, Y., K. Manova, and R. Benezra. 1997. Each member of the Id gene family exhibits a unique expression pattern in mouse gastrulation and neurogenesis. Dev. Dyn. 208:92–106.
   PubMed Web of Science ®Google Scholar
• Jen, Y., K. Manova, and R. Benezra. 1996. Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev. Dyn. 207:235–252.
   PubMed Web of Science ®Google Scholar
• Kim, E. S., A. Serur, J. Huang, C. A. Manley, K. W. McCrudden, J. S. Frischer, S. Z. Soffer, L. Ring, T. New, S. Zabski, J. S. Rudge, J. Holash, G. D. Yancopoulos, J. J. Kandel, and D. J. Yamashiro. 2002. Potent VEGF blockade causes regression of coopted vessels in a model of neuroblastoma. Proc. Natl. Acad. Sci. USA 99:11399–11404.
   PubMed Web of Science ®Google Scholar
• Lasorella, A., R. Boldrini, C. Dominici, A. Donfrancesco, Y. Yokota, A. Inserra, and A. Iavarone. 2002. Id2 is critical for cellular proliferation and is the oncogenic effector of N-myc in human neuroblastoma. Cancer Res. 62:301–306.
   PubMedGoogle Scholar
• Lasorella, A., A. Iavarone, and M. A. Israel. 1996. Id2 specifically alters regulation of the cell cycle by tumor suppressor proteins. Mol. Cell. Biol. 16:2570–2578.
   PubMedGoogle Scholar
• Lasorella, A., M. Noseda, M. Beyna, Y. Yokota, and A. Iavarone. 2000. Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature 407:592–598.
   PubMedGoogle Scholar
• Lasorella, A., T. Uo, and A. Iavarone. 2001. Id proteins at the cross-road of development and cancer. Oncogene 20:8326–8333.
   PubMed Web of Science ®Google Scholar
• Laughner, E., P. Taghavi, K. Chiles, P. C. Mahon, and G. L. Semenza. 2001. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol. Cell. Biol. 21:3995–4004.
   PubMed Web of Science ®Google Scholar
• Lee, E. Y.-H. P., C.-Y. Chang, N. Hu, Y.-C. J. Wang, C.-C. Iai, K. Herrup, W.-H. Lee, and A. Bradley. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and hematopoesis. Nature 359:288–294.
   PubMed Web of Science ®Google Scholar
• Lentini, L., L. Pipitone, and A. Di Leonardo. 2002. Functional inactivation of pRB results in aneuploid mammalian cells after release from a mitotic block. Neoplasia 4:380–387.
   PubMedGoogle Scholar
• Liu, J., C. Lin, A. Gleiberman, K. A. Ohgi, T. Herman, H. P. Huang, M. J. Tsai, and M. G. Rosenfeld. 2001. Tbx19, a tissue-selective regulator of POMC gene expression. Proc. Natl. Acad. Sci. USA 98:8674–8679.
   PubMed Web of Science ®Google Scholar
• Lyden, D., K. Hattori, S. Dias, C. Costa, P. Blaikie, L. Butros, A. Chadburn, B. Heissig, W. Marks, L. Witte, Y. Wu, D. Hicklin, Z. Zhu, N. R. Hackett, R. G. Crystal, M. A. Moore, K. A. Hajjar, K. Manova, R. Benezra, and S. Rafii. 2001. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat. Med. 7:1194–1201.
   PubMed Web of Science ®Google Scholar
• Lyden, D., A. Z. Young, D. Zagzag, W. Yan, W. Gerald, R. O'Reilly, B. L. Bader, R. O. Hynes, Y. Zhuang, K. Manova, and R. Benezra. 1999. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401:670–677.
   PubMed Web of Science ®Google Scholar
• Maandag, E. C., M. van der Valk, M. Vlaar, C. Feltkamp, J. O'Brien, M. van Roon, N. van der Lugt, A. Berns, and H. te Riele. 1994. Developmental rescue of an embryonic-lethal mutation in the retinoblastoma gene in chimeric mice. EMBO J. 13:4260–4268.
   PubMed Web of Science ®Google Scholar
• Mori, S., S. I. Nishikawa, and Y. Yokota. 2000. Lactation defect in mice lacking the helix-loop-helix inhibitor Id2. EMBO J. 19:5772–5781.
   PubMed Web of Science ®Google Scholar
• Moynahan, M. E., and M. Jasin. 1997. Loss of heterozygosity induced by a chromosomal double-strand break. Proc. Natl. Acad. Sci. USA 94:8988–8993.
   PubMed Web of Science ®Google Scholar
• Nikiforov, M. A., N. Popov, I. Kotenko, M. Henriksson, and M. D. Cole. 2003. The Mad and Myc basic domains are functionally equivalent. J. Biol. Chem. 278:11094–11099.
   PubMedGoogle Scholar
• Nikitin, A., and W. H. Lee. 1996. Early loss of the retinoblastoma gene is associated with impaired growth inhibitory innervation during melanotroph carcinogenesis in Rb+/− mice. Genes Dev. 10:1870–1879.
   PubMedGoogle Scholar
• Nishimori, H., Y. Sasaki, K. Yoshida, H. Irifune, H. Zembutsu, T. Tanaka, T. Aoyama, T. Hosaka, S. Kawaguchi, T. Wada, J. Hata, J. Toguchida, Y. Nakamura, and T. Tokino. 2002. The Id2 gene is a novel target of transcriptional activation by EWS-ETS fusion proteins in Ewing family tumors. Oncogene 21:8302–8309.
   PubMedGoogle Scholar
• Norton, J. D., R. W. Deed, G. Craggs, and F. Sablitzky. 1998. Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol. 8:58–65.
   PubMedGoogle Scholar
• Ochoa, A. L., N. A. Mitchner, C. D. Paynter, R. E. Morris, and N. Ben-Jonathan. 2000. Vascular endothelial growth factor in the rat pituitary: differential distribution and regulation by estrogen. J. Endocrinol. 165:483–492.
   PubMedGoogle Scholar
• Pelengaris, S., M. Khan, and G. I. Evan. 2002. Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell 109:321–334.
   PubMed Web of Science ®Google Scholar
• Piao, Z., H. Kim, B. K. Jeon, W. J. Lee, and C. Park. 1997. Relationship between loss of heterozygosity of tumor suppressor genes and histologic differentiation in hepatocellular carcinoma. Cancer 80:865–872.
   PubMedGoogle Scholar
• Poulin, G., M. Lebel, M. Chamberland, F. W. Paradis, and J. Drouin. 2000. Specific protein-protein interaction between basic helix-loop-helix transcription factors and homeoproteins of the Pitx family. Mol. Cell. Biol. 20:4826–4837.
   PubMed Web of Science ®Google Scholar
• Poulin, G., B. Turgeon, and J. Drouin. 1997. NeuroD1/beta2 contributes to cell-specific transcription of the proopiomelanocortin gene. Mol. Cell. Biol. 17:6673–6682.
   PubMed Web of Science ®Google Scholar
• Raetz, E. A., M. K. Kim, P. Moos, M. Carlson, C. Bruggers, D. K. Hooper, L. Foot, T. Liu, R. Seeger, and W. L. Carroll. 2003. Identification of genes that are regulated transcriptionally by Myc in childhood tumors. Cancer 98:841–853.
   PubMedGoogle Scholar
• Ross, S. E., M. E. Greenberg, and C. D. Stiles. 2003. Basic helix-loop-helix factors in cortical development. Neuron 39:13–25.
   PubMed Web of Science ®Google Scholar
• Russell, R. G., A. Lasorella, L. E. Dettin, and A. Iavarone. 2004. Id2 drives differentiation and suppresses tumor formation in the intestinal epithelium. Cancer Res. 64:7220–7225.
   PubMed Web of Science ®Google Scholar
• Ruzinova, M. B., and R. Benezra. 2003. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13:410–418.
   PubMed Web of Science ®Google Scholar
• Ruzinova, M. B., R. A. Schoer, W. Gerald, J. E. Egan, P. P. Pandolfi, S. Rafii, K. Manova, V. Mittal, and R. Benezra. 2003. Effect of angiogenesis inhibition by Id loss and the contribution of bone-marrow-derived endothelial cells in spontaneous murine tumors. Cancer Cell 4:277–289.
   PubMed Web of Science ®Google Scholar
• Scully, K. M., and M. G. Rosenfeld. 2002. Pituitary development: regulatory codes in mammalian organogenesis. Science 295:2231–2235.
   PubMed Web of Science ®Google Scholar
• Thiele, C. J., C. P. Reynolds, and M. A. Israel. 1985. Decreased expression of N-myc precedes retinoic acid-induced morphological differentiation of human neuroblastoma. Nature 313:404–406.
   PubMed Web of Science ®Google Scholar
• Toma, J. G., H. El-Bizri, F. Barnabe-Heider, R. Aloyz, and F. D. Miller. 2000. Evidence that helix-loop-helix proteins collaborate with retinoblastoma tumor suppressor protein to regulate cortical neurogenesis. J. Neurosci. 20:7648–7656.
   PubMedGoogle Scholar
• Treins, C., S. Giorgetti-Peraldi, J. Murdaca, G. L. Semenza, and E. Van Obberghen. 2002. Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J. Biol. Chem. 277:27975–27981.
   PubMed Web of Science ®Google Scholar
• Trinh, E., E. L. Denchi, and K. Helin. 2004. Naturally death-resistant precursor cells revealed as the origin of retinoblastoma. Cancer Cell 5:513–515.
   PubMedGoogle Scholar
• Tsai, K. Y., D. MacPherson, D. A. Rubinson, A. Y. Nikitin, R. Bronson, K. L. Mercer, D. Crowley, and T. Jacks. 2002. ARF mutation accelerates pituitary tumor development in Rb+/− mice. Proc. Natl. Acad. Sci. USA 99:16865–16870.
   PubMedGoogle Scholar
• Vandeputte, D. A., D. Troost, S. Leenstra, H. Ijlst-Keizers, M. Ramkema, D. A. Bosch, F. Baas, N. K. Das, and E. Aronica. 2002. Expression and distribution of id helix-loop-helix proteins in human astrocytic tumors. Glia 38:329–338.
   PubMed Web of Science ®Google Scholar
• Viloria-Petit, A., L. Miquerol, J. L. Yu, M. Gertsenstein, C. Sheehan, L. May, J. Henkin, C. Lobe, A. Nagy, R. S. Kerbel, and J. Rak. 2003. Contrasting effects of VEGF gene disruption in embryonic stem cell-derived versus oncogene-induced tumors. EMBO J. 22:4091–4102.
   PubMedGoogle Scholar
• Volpert, O. V., R. Pili, H. A. Sikder, T. Nelius, T. Zaichuk, C. Morris, C. B. Shiflett, M. K. Devlin, K. Conant, and R. M. Alani. 2002. Id1 regulates angiogenesis through transcriptional repression of thrombospondin-1. Cancer Cell 2:473–483.
   PubMedGoogle Scholar
• Vooijs, M., M. van der Valk, H. te Riele, and A. Berns. 1998. Flp-mediated tissue-specific inactivation of the retinoblastoma tumor suppressor gene in the mouse. Oncogene 17:1–12.
   PubMed Web of Science ®Google Scholar
• Williams, B. O., E. M. Schmitt, L. Remington, R. T. Bronson, D. M. Albert, R. A. Weinberg, and T. Jacks. 1994. Extensive contribution of Rb-deficient cells to adult chimeric mice with limited histopathological consequences. EMBO J. 13:4251–4259.
   PubMed Web of Science ®Google Scholar
• Yancopoulos, G. D., S. Davis, N. W. Gale, J. S. Rudge, S. J. Wiegand, and J. Holash. 2000. Vascular-specific growth factors and blood vessel formation. Nature 407:242–248.
   PubMed Web of Science ®Google Scholar
• Ying, Q. L., J. Nichols, I. Chambers, and A. Smith. 2003. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115:281–292.
   PubMed Web of Science ®Google Scholar
• Yokota, Y., A. Mansouri, S. Mori, S. Sugawara, S. Adachi, S. Nishikawa, and P. Gruss. 1999. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397:702–706.
   PubMed Web of Science ®Google Scholar
• Zheng, L., A. Flesken-Nikitin, P. L. Chen, and W. H. Lee. 2002. Deficiency of retinoblastoma gene in mouse embryonic stem cells leads to genetic instability. Cancer Res. 62:2498–2502.
   PubMed Web of Science ®Google Scholar
• Zundel, W., C. Schindler, D. Haas-Kogan, A. Koong, F. Kaper, E. Chen, A. R. Gottschalk, H. E. Ryan, R. S. Johnson, A. B. Jefferson, D. Stokoe, and A. J. Giaccia. 2000. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev. 14:391–396.
   PubMed Web of Science ®Google Scholar