An ID2-dependent mechanism for VHL inactivation in cancer

Nature

Volumn 529, Issue 7585, 2016, Pages 172-177

  Lee, Sang Bae ^a   Frattini, Veronique ^a   Bansal, Mukesh ^a   Castano, Angelica M ^a   Sherman, Dan ^b   Hutchinson, Keino ^b   Bruce, Jeffrey N ^a   Califano, Andrea ^a   Liu, Guangchao ^a   Cardozo, Timothy ^b   Iavarone, Antonio ^a   Lasorella, Anna ^a  

^a Columbia University ^*  (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CULLIN; CULLIN 2; HYPOXIA INDUCIBLE FACTOR 2ALPHA; INHIBITOR OF DIFFERENTIATION 2; PHOSPHOTRANSFERASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; THREONINE; THREONINE 27; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CUL2 PROTEIN, HUMAN; DYRK KINASE; EGLN2 PROTEIN, HUMAN; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; ID2 PROTEIN, HUMAN; OXYGEN; PHOSPHOTHREONINE; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE;

CANCER; ENZYME ACTIVITY; GENE EXPRESSION; HYPOXIA; OXYGEN; PROTEIN; TUMOR;

ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; DEGRADATION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; GLIOBLASTOMA; HUMAN; HUMAN CELL; OXYGEN SENSING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; STIMULATION; TUMOR GROWTH; UBIQUITINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER STEM CELL; DRUG SCREENING; MALE; METABOLISM; MOUSE; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CELL LINE, TUMOR; CULLIN PROTEINS; GLIOBLASTOMA; HUMANS; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; INHIBITOR OF DIFFERENTIATION PROTEIN 2; MALE; MICE; NEOPLASTIC STEM CELLS; OXYGEN; PHOSPHORYLATION; PHOSPHOTHREONINE; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; UBIQUITINATION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84954235083     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16475     Document Type: Article

References (53)

1. Keith, B., Johnson, R. S., Simon, M. C. HIF1 and HIF2 : sibling rivalry in hypoxic tumour growth and progression. Nature Rev. Cancer 12, 9-22 (2012).
2. Gordan, J. D., Bertout, J. A., Hu, C. J., Diehl, J. A., Simon, M. C. HIF-2 promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 11, 335-347 (2007).
3. Kondo, K., Kim, W. Y., Lechpammer, M., Kaelin, W. G., Jr. Inhibition of HIF2 is sufficient to suppress pVHL-defective tumor growth. PLoS Biol. 1, E83 (2003).
4. Li, Z. et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 15, 501-513 (2009).
5. Pietras, A. et al. HIF-2 maintains an undifferentiated state in neural crest-like human neuroblastoma tumor-initiating cells. Proc. Natl Acad. Sci. USA 106, 16805-16810 (2009).
6. Lasorella, A., Benezra, R., Iavarone, A. The ID proteins: master regulators of cancer stem cells and tumour aggressiveness. Nature Rev. Cancer 14, 77-91 (2014).
7. Perk, J., Iavarone, A., Benezra, R. Id family of helix-loop-helix proteins in cancer. Nature Rev. Cancer 5, 603-614 (2005).
8. Lasorella, A., Rothschild, G., Yokota, Y., Russell, R. G., Iavarone, A. Id2 mediates tumor initiation, proliferation, and angiogenesis in Rb mutant mice. Mol. Cell. Biol. 25, 3563-3574 (2005).
9. Niola, F. et al. Mesenchymal high-grade glioma is maintained by the ID-RAP1 axis. J. Clin. Invest. 123, 405-417 (2013).
10. Vandeputte, D. A. et al. Expression and distribution of id helix-loop-helix proteins in human astrocytic tumors. Glia 38, 329-338 (2002).
11. Hara, E., Hall, M., Peters, G. Cdk2-dependent phosphorylation of Id2 modulates activity of E2A-related transcription factors. EMBO J. 16, 332-342 (1997).
12. Nam, H. S., Benezra, R. High levels of Id1 expression define B1 type adult neural stem cells. Cell Stem Cell 5, 515-526 (2009).
13. Niola, F. et al. Id proteins synchronize stemness and anchorage to the niche of neural stem cells. Nature Cell Biol. 14, 477-487 (2012).
14. Himpel, S. et al. Specificity determinants of substrate recognition by the protein kinase DYRK1A. J. Biol. Chem. 275, 2431-2438 (2000).
15. Lee, K., Deng, X., Friedman, E. Mirk protein kinase is a mitogen-activated protein kinase substrate that mediates survival of colon cancer cells. Cancer Res. 60, 3631-3637 (2000).
16. Göckler, N. et al. Harmine specifically inhibits protein kinase DYRK1A and interferes with neurite formation. FEBS J. 276, 6324-6337 (2009).
17. Himpel, S. et al. Identification of the autophosphorylation sites and characterization of their effects in the protein kinase DYRK1A. Biochem. J. 359, 497-505 (2001).
18. Kaelin, W. G. Jr & Ratcliffe, P. J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30, 393-402 (2008).
19. Semenza, G. L. HIF-1, O(2), and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 107, 1-3 (2001).
20. Warnecke, C. et al. Differentiating the functional role of hypoxia-inducible factor (HIF)-1 and HIF-2 (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2 target gene in Hep3B and Kelly cells. FASEB J. 18, 1462-1464 (2004).
21. Kershaw, N. J., Babon, J. J. VHL: cullin-g the hypoxic response. Structure 23, 435-436 (2015).
22. Nguyen, H. C., Yang, H., Fribourgh, J. L., Wolfe, L. S., Xiong, Y. Insights into Cullin-RING E3 ubiquitin ligase recruitment: structure of the VHL-EloBC-Cul2 complex. Structure 23, 441-449 (2015).
23. Kamura, T. et al. Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science 284, 657-661 (1999).
24. Ohta, T., Michel, J. J., Schottelius, A. J., Xiong, Y. ROC1, a homolog of APC11, represents a family of cullin partners with an associated ubiquitin ligase activity. Mol. Cell 3, 535-541 (1999).
25. Giorgi, F. M. et al. Inferring protein modulation from gene expression data using conditional mutual information. PLoS ONE 9, e109569 (2014).
26. Alvarez, M. J., Giorgi, F. M., Califano, A. Using viper, a package for virtual inference of protein-activity by enriched regulon analysis. Bioconductor, 1-14 (2014).
27. Löfstedt, T. et al. Induction of ID2 expression by hypoxia-inducible factor-1: a role in dedifferentiation of hypoxic neuroblastoma cells. J. Biol. Chem. 279, 39223-39231 (2004).
28. Chakrabarti, L., Galdzicki, Z., Haydar, T. F. Defects in embryonic neurogenesis and initial synapse formation in the forebrain of the Ts65Dn mouse model of Down syndrome. J. Neurosci. 27, 11483-11495 (2007).
29. Contestabile, A. et al. Cell cycle alteration and decreased cell proliferation in the hippocampal dentate gyrus and in the neocortical germinal matrix of fetuses with Down syndrome and in Ts65Dn mice. Hippocampus 17, 665-678 (2007).
30. Guimeá, J. et al. A human homologue of Drosophila minibrain (MNB) is expressed in the neuronal regions affected in Down syndrome and maps to the critical region. Hum. Mol. Genet. 5, 1305-1310 (1996).
31. Hibaoui, Y. et al. Modelling and rescuing neurodevelopmental defect of Down syndrome using induced pluripotent stem cells from monozygotic twins discordant for trisomy 21. EMBO Mol. Med. 6, 259-277 (2014).
32. Aranda, S., Laguna, A., de la Luna, S. DYRK family of protein kinases: evolutionary relationships, biochemical properties, and functional roles. FASEB J. 25, 449-462 (2011).
33. Becker, W. Emerging role of DYRK family protein kinases as regulators of protein stability in cell cycle control. Cell Cycle 11, 3389-3394 (2012).
34. Hämmerle, B. et al. Transient expression of Mnb/Dyrk1a couples cell cycle exit and differentiation of neuronal precursors by inducing p27KIP1 expression and suppressing NOTCH signaling. Development 138, 2543-2554 (2011).
35. Litovchick, L., Florens, L. A., Swanson, S. K., Washburn, M. P., DeCaprio, J. A. DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly. Genes Dev. 25, 801-813 (2011).
36. Park, J. et al. Dyrk1A phosphorylates p53 and inhibits proliferation of embryonic neuronal cells. J. Biol. Chem. 285, 31895-31906 (2010).
37. Yabut, O., Domogauer, J., D'Arcangelo, G. Dyrk1A overexpression inhibits proliferation and induces premature neuronal differentiation of neural progenitor cells. J. Neurosci. 30, 4004-4014 (2010).
38. Lauth, M. et al. DYRK1B-dependent autocrine-to-paracrine shift of Hedgehog signaling by mutant RAS. Nature Struct. Mol. Biol. 17, 718-725 (2010).
39. Mao, J. et al. Regulation of Gli1 transcriptional activity in the nucleus by Dyrk1. J. Biol. Chem. 277, 35156-35161 (2002).
40. Yang, E. J., Ahn, Y. S., Chung, K. C. Protein kinase Dyrk1 activates cAMP response element-binding protein during neuronal differentiation in hippocampal progenitor cells. J. Biol. Chem. 276, 39819-39824 (2001).
41. Pozo, N. et al. Inhibition of DYRK1A destabilizes EGFR and reduces EGFRdependent glioblastoma growth. J. Clin. Invest. 123, 2475-2487 (2013)
42. Carro, M. S. et al. The transcriptional network for mesenchymal transformation of brain tumours. Nature 463, 318-325 (2010).
43. Reynolds, B. A., Weiss, S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175, 1-13 (1996).
44. Deleyrolle, L. P. et al. Determination of somatic and cancer stem cell self-renewing symmetric division rate using sphere assays. PLoS One. 6, e15844 (2011).
45. Tropepe, V. et al. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev. Biol. 208, 166-188 (1999).
46. Miînea, C. P., Lienhard, G. E. Stoichiometry of site-specific protein phosphorylation estimated with phosphopeptide-specific antibodies. Biotechniques 34, 828-831 (2003).
47. Bordner, A. J., Abagyan, R. Ab initio prediction of peptide-MHC binding geometry for diverse class I MHC allotypes. Proteins 63, 512-526 (2006).
48. Abagyan, R., Totrov, M. Biased probability Monte Carlo conformational searches and electrostatic calculations for peptides and proteins. J. Mol. Biol. 235, 983-1002 (1994).
49. Almond, D., Cardozo, T. Assessment of immunologically relevant dynamic tertiary structural features of the HIV-1 V3 loop crown R2 sequence by ab initio folding. J. Vis. Exp. 43, 2118 (2010).
50. Zhao, X. et al. The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myc oncoprotein. Nature Cell Biol. 10, 643-653 (2008).
51. Cawthorne, C., Swindell, R., Stratford, I. J., Dive, C., Welman, A. Comparison of doxycycline delivery methods for Tet-inducible gene expression in a subcutaneous xenograft model. J. Biomol. Tech. 18, 120-123 (2007).
52. Zhao, X. et al. The N-Myc-DLL3 cascade is suppressed by the ubiquitin ligase Huwe1 to inhibit proliferation and promote neurogenesis in the developing brain. Dev. Cell 17, 210-221 (2009).
53. Wang, K. et al. Genome-wide identification of post-translational modulators of transcription factor activity in human B cells. Nature Biotechnol. 27, 829-837 (2009).