Suppression of tumor angiogenesis by targeting the protein neddylation pathway

Cell Death and Disease

Volumn 5, Issue 2, 2014, Pages

  Yao, W T ^a,b   Wu, J F ^a,b   Yu, G Y ^a,b   Wang, R ^c   Wang, K ^d   Li, L H ^a   Chen, P ^a   Jiang, Y N ^a,b   Cheng, H ^a   Lee, H W ^e   Yu, J ^e   Qi, H ^f   Yu, X J ^a   Wang, P ^c   Chu, Y W ^b   Yang, M ^f   Hua, Z C ^d   Ying, H Q ^g   Hoffman, R M ^h,i   Jeong, L S ^e   Jia, L J ^a,b   more..

^a FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^b FUDAN UNIVERSITY   (China)

^c EAST CHINA NORMAL UNIVERSITY   (China)

^d NANJING UNIVERSITY   (China)

^e Seoul National University   (South Korea)

^f AntiCancer Beijing Co Ltd   (China)

^g UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^h UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

ⁱ ANTICANCER INC   (United States)

Author keywords

cullinRING ligase; MLN4924; neddylation; tumor angiogenesis

Indexed keywords

CULLIN; PEVONEDISTAT; SMALL INTERFERING RNA;

ANGIOGENESIS; ANGIOGENESIS ASSAY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL CYCLE ARREST; CELL DEATH; CONTROLLED STUDY; DNA DAMAGE; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MALE; METASTASIS; NEDDYLATION; NEOPLASM; NONHUMAN; PANCREAS CANCER; PHENOTYPE; PRIORITY JOURNAL; RAT; TUMOR GROWTH;

ANGIOGENESIS INHIBITORS; ANIMALS; APOPTOSIS; CARRIER PROTEINS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; CULLIN PROTEINS; CYCLOPENTANES; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PANCREATIC NEOPLASMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PYRIMIDINES; RATS; RATS, SPRAGUE-DAWLEY; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; TIME FACTORS; TISSUE CULTURE TECHNIQUES; TRANSFECTION; TUMOR BURDEN; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84896750639     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.21     Document Type: Article

References (58)

1. Rabut G, Peter M. Function and regulation of protein neddylation. 'Protein modifications: Beyond the usual suspects' review series. EMBO Rep 2008; 9: 969-976.
2. Xirodimas DP. Novel substrates and functions for the ubiquitin-like molecule NEDD8. Biochem Soc Trans 2008; 36(Pt 5): 802-806.
3. Sakata E, Yamaguchi Y, Miyauchi Y, Iwai K, Chiba T, Saeki Y et al. Direct interactions between NEDD8 and ubiquitin E2 conjugating enzymes upregulate cullin-based E3 ligase activity. Nat Struct Mol Biol 2007; 14: 167-168.
4. Wu JT, Lin HC, Hu YC, Chien CT. Neddylation and deneddylation regulate Cul1 and Cul3 protein accumulation. Nat Cell Biol 2005; 7: 1014-1020.
5. Nalepa G, Rolfe M, Harper JW. Drug discovery in the ubiquitin-proteasome system. Nat Rev Drug Discov 2006; 5: 596-613.
6. Jia L, Sun Y. SCF E3 ubiquitin ligases as anticancer targets. Curr Cancer Drug Targets 2011; 11: 347-356.
7. Xirodimas DP, Saville MK, Bourdon JC, Hay RT, Lane DP. Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell 2004; 118: 83-97.
8. Embade N, Fernandez-Ramos D, Varela-Rey M, Beraza N, Sini M, Gutierrez de Juan V et al. Murine double minute 2 regulates Hu antigen R stability in human liver and colon cancer through NEDDylation. Hepatology 2012; 55: 1237-1248.
9. Tanaka T, Nakatani T, Kamitani T. Inhibition of NEDD8-conjugation pathway by novel molecules: Potential approaches to anticancer therapy. Mol Oncol 2012; 6: 267-275.
10. Wang M, Medeiros BC, Erba HP, DeAngelo DJ, Giles FJ, Swords RT. Targeting protein neddylation: A novel therapeutic strategy for the treatment of cancer. Expert Opin Ther Target 2011; 15: 253-264.
11. Soucy TA, Dick LR, Smith PG, Milhollen MA, Brownell JE. The NEDD8 conjugation pathway and its relevance in cancer biology and therapy. Genes Cancer 2010; 1 716.
12. Soucy TA, Smith PG, Milhollen MA, Berger AJ, Gavin JM, Adhikari S et al. An inhibitor of NEDD8-Activating enzyme as a new approach to treat cancer. Nature 2009; 458: 732-736.
13. Nawrocki ST, Griffin P, Kelly KR, Carew JS. MLN4924: A novel first-in-class inhibitor of NEDD8-Activating enzyme for cancer therapy. Expert Opin Investig Drugs 2012; 21 1573.
14. Brownell JE, Sintchak MD, Gavin JM, Liao H, Bruzzese FJ, Bump NJ et al. Substrate-Assisted inhibition of ubiquitin-like protein-Activating enzymes: The NEDD8 E1 inhibitor MLN4924 forms a NEDD8-AMP mimetic in situ. Mol Cell 2010; 37: 102-111.
15. Luo Z, Yu G, Lee HW, Li L, Wang L, Yang D et al. The Nedd8-Activating enzyme inhibitor MLN4924 induces autophagy and apoptosis to suppress liver cancer cell growth. Cancer Res 2012; 72: 3360-3371.
16. Jia L, Li H, Sun Y. Induction of p21-dependent senescence by an NAE inhibitor, MLN4924, as a mechanism of growth suppression. Neoplasia 2011; 13: 561-569.
17. Milhollen MA, Traore T, Adams-Duffy J, Thomas MP, Berger AJ, Dang L et al. MLN4924, a NEDD8-Activating enzyme inhibitor, is active in diffuse large B-cell lymphoma models: Rationale for treatment of NF-{kappa}B-dependent lymphoma. Blood 2010; 116 1523.
18. Nawrocki ST, Kelly KR, Smith PG, Espitia CM, Possemato A, Beausoleil SA et al. Disrupting protein NEDDylation with MLN4924 is a novel strategy to target cisplatin resistance in ovarian cancer. Clin Cancer Res 2013; 19: 3577-3590.
19. Wei D, Li H, Yu J, Sebolt JT, Zhao L, Lawrence TS et al. Radiosensitization of human pancreatic cancer cells by MLN4924, an investigational NEDD8-Activating enzyme inhibitor. Cancer Res 2012; 72: 282-293.
20. Pan WW, Zhou JJ, Yu C, Xu Y, Guo LJ, Zhang HY et al. Ubiquitin E3 ligase CRL4CDT2/DCAF2 as a potential chemotherapeutic target for ovarian surface epithelial cancer. J Biol Chem 2013; 288: 29680-29691.
21. Blank JL, Liu XJ, Cosmopoulos K, Bouck DC, Garcia K, Bernard H et al. Novel DNA damage checkpoints mediating cell death induced by the NEDD8-Activating enzyme inhibitor MLN4924. Cancer Res 2013; 73: 225-234.
22. Mackintosh C, Garcia-Dominguez DJ, Ordonez JL, Ginel-Picardo A, Smith PG, Sacristan MP et al. WEE1 accumulation and deregulation of S-phase proteins mediate MLN4924 potent inhibitory effect on Ewing sarcoma cells. Oncogene 2013; 32: 1441-1451.
23. Milhollen MA, Narayanan U, Soucy TA, Veiby PO, Smith PG, Amidon B. Inhibition of NEDD8-Activating enzyme induces rereplication and apoptosis in human tumor cells consistent with deregulating CDT1 turnover. Cancer Res 2011; 71: 3042-3051.
24. Swords RT, Kelly KR, Smith PG, Garnsey JJ, Mahalingam D, Medina E et al. Inhibition of NEDD8-Activating enzyme: A novel approach for the treatment of acute myeloid leukemia. Blood 2010; 115: 3796-3800.
25. Lin JJ, Milhollen MA, Smith PG, Narayanan U, Dutta A. NEDD8-Targeting drug MLN4924 elicits DNA rereplication by stabilizing Cdt1 in S phase, triggering checkpoint activation, apoptosis, and senescence in cancer cells. Cancer Res 2010; 70: 10310-10320.
26. Jazaeri AA, Shibata E, Park J, Bryant JL, Conaway MR, Modesitt SC et al. Overcoming platinum resistance in preclinical models of ovarian cancer using the neddylation inhibitor MLN4924. Mol Cancer Ther 2013; 12: 1958-1967.
27. Yang D, Tan M, Wang G, Sun Y. The p21-dependent radiosensitization of human breast cancer cells by MLN4924, an investigational inhibitor of NEDD8 activating enzyme. PLoS One 2012; 7: E34079.
28. Kee Y, Huang M, Chang S, Moreau LA, Park E, Smith PG et al. Inhibition of the Nedd8 system sensitizes cells to DNA interstrand cross-linking agents. Mol Cancer Res 2012; 10 377.
29. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol 2002 (6 Suppl 16): 15-18.
30. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144 674.
31. Weis SM, Cheresh DA. Tumor angiogenesis: Molecular pathways and therapeutic targets. Nat Med 2011; 17: 1359-1370.
32. Kerbel RS. Tumor angiogenesis. N Engl J Med 2008; 358: 2039-2049.
33. Yang M, Jiang P, Hoffman RM. Whole-body subcellular multicolor imaging of tumor-host interaction and drug response in real time. Cancer Res 2007; 67: 5195-5200.
34. Yang M, Baranov E, Moossa AR, Penman S, Hoffman RM. Visualizing gene expression by whole-body fluorescence imaging. Proc Natl Acad Sci USA 2000; 97: 12278-12282.
35. Hoffman RM, Yang M. Whole-body imaging with fluorescent proteins. Nat Protoc 2006; 1 1438.
36. Kurz T, Chou YC, Willems AR, Meyer-Schaller N, Hecht ML, Tyers M et al. Dcn1 functions as a scaffold-Type E3 ligase for cullin neddylation. Mol Cell 2008; 29: 23-35.
37. Kurz T, Ozlu N, Rudolf F, O'Rourke SM, Luke B, Hofmann K et al. The conserved protein DCN-1/Dcn1p is required for cullin neddylation in C. elegans and S. cerevisiae. Nature 2005; 435: 1257-1261.
38. Morimoto M, Nishida T, Nagayama Y, Yasuda H. Nedd8-modification of Cul1 is promoted by Roc1 as a Nedd8-E3 ligase and regulates its stability. Biochem Biophys Res Commun 2003; 301: 392-398.
39. Tan M, Zhao Y, Kim SJ, Liu M, Jia L, Saunders TL et al. SAG/RBX2/ROC2 E3 ubiquitin ligase is essential for vascular and neural development by targeting NF1 for degradation. Dev Cell 2011; 21: 1062-1076.
40. Wang R, Wang Y, Liu N, Ren C, Jiang C, Zhang K et al. FBW7 regulates endothelial functions by targeting KLF2 for ubiquitination and degradation. Cell Res 2013; 23 819.
41. Chen Y, Yang Z, Meng M, Zhao Y, Dong N, Yan H et al. Cullin mediates degradation of RhoA through evolutionarily conserved BTB adaptors to control actin cytoskeleton structure and cell movement. Mol Cell 2009; 35: 841-855.
42. Jia L, Yang J, Hao X, Zheng M, He H, Xiong X et al. Validation of SAG/RBX2/ROC2 E3 ubiquitin ligase as an anticancer and radiosensitizing target. Clin Cancer Res 2010; 16 824.
43. Yang D, Li L, Liu H, Wu L, Luo Z, Li H et al. Induction of autophagy and senescence by knockdown of ROC1 E3 ubiquitin ligase to suppress the growth of liver cancer cells. Cell Death Differ 2013; 20: 235-247.
44. Jia L, Bickel JS, Wu J, Morgan MA, Li H, Yang J et al. RBX1 (RING box protein 1) E3 ubiquitin ligase is required for genomic integrity by modulating DNA replication licensing proteins. J Biol Chem 2011; 286: 3379-3386.
45. Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007; 8: 464-478.
46. Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature 2005; 438: 967-974.
47. Otrock ZK, Mahfouz RA, Makarem JA, Shamseddine AI. Understanding the biology of angiogenesis: Review of the most important molecular mechanisms. Blood Cells Mol Dis 2007; 39: 212-220.
48. Tan M, Li H, Sun Y. Endothelial deletion of Sag/Rbx2/Roc2 E3 ubiquitin ligase causes embryonic lethality and blocks tumor angiogenesis. Oncogene 2013; e-pub ahead of print 11 November 2013; doi:10.1038/onc.2013.473.
49. Lee HW, Nam SK, Choi WJ, Kim HO, Jeong LS. Stereoselective synthesis of MLN4924, an inhibitor of NEDD8-Activating enzyme. J Org Chem 2011; 76: 3557-3561.
50. Wang B, Sun J, Kitamoto S, Yang M, Grubb A, Chapman HA et al. Cathepsin S controls angiogenesis and tumor growth via matrix-derived angiogenic factors. J Biol Chem 2006 6020-6029.
51. Brooks PC, Montgomery AM, Rosenfeld M, Reisfeld RA, Hu T, Klier G et al. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 1994; 79: 1157-1164.
52. Chen J, Wei D, Zhuang H, Qiao Y, Tang B, Zhang X et al. Proteomic screening of anaerobically regulated promoters from Salmonella and its antitumor applications. Mol Cell Proteomics 2011; 10: M111 009399.
53. Malinda KM. In vivo matrigel migration and angiogenesis assay. Methods Mol Biol 2009 287-294.
54. Hoffman RM. Orthotopic metastatic mouse models for anticancer drug discovery and evaluation: A bridge to the clinic. Invest New Drugs 1999; 17: 343-359.
55. Bockbrader KM, Tan M, Sun Y. A small molecule Smac-mimic compound induces apoptosis and sensitizes TRAIL-And etoposide-induced apoptosis in breast cancer cells. Oncogene 2005; 24: 7381-7388.
56. Shan T, Ma J, Ma Q, Guo K, Guo J, Li X et al. beta2-AR-HIF-1alpha: A novel regulatory axis for stress-induced pancreatic tumor growth and angiogenesis. Curr Mol Med 2013; 13 1034.
57. Wang Q, Mora-Jensen H, Weniger MA, Perez-Galan P, Wolford C, Hai T et al. ERAD inhibitors integrate ER stress with an epigenetic mechanism to activate BH3-only protein NOXA in cancer cells. Proc Natl Acad Sci USA 2009; 106: 2200-2205.
58. Tang QL, Xie XB, Wang J, Chen Q, Han AJ, Zou CY et al. Glycogen synthase kinase-beta, NF-kappaB signaling, and tumorigenesis of human osteosarcoma. J Natl Cancer Inst 2012; 104: 749-763.