The APC/C E3 ligase complex activator fzr1 restricts braf oncogenic function

Cancer Discovery

Volumn 7, Issue 4, 2017, Pages 424-441

  Wan, Lixin ^a,b   Chen, Ming ^a   Cao, Juxiang ^c   Dai, Xiangpeng ^a   Yin, Qing ^b   Zhang, Jinfang ^a   Song, Su Jung ^a   Lu, Ying ^a   Liu, Jing ^a,d   Inuzuka, Hiroyuki ^a   Katon, Jesse M ^a   Berry, Kelsey ^a   Fung, Jacqueline ^a   Ng, Christopher ^a   Liu, Pengda ^a   Song, Min Sup ^e   Xue, Lian ^b   Bronson, Roderick T ^a   Kirschner, Marc W ^a   Cui, Rutao ^c   Pandolfi, Pier Paolo ^a   Wei, Wenyi ^a   more..

^a HARVARD MEDICAL SCHOOL   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d XI'AN JIAOTONG UNIVERSITY   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; ANTIBODY; B RAF KINASE; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; DIMER; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE INHIBITOR; PROTEIN KINASE B; RAF PROTEIN; UBIQUITIN PROTEIN LIGASE E3; APC PROTEIN; APC PROTEIN, HUMAN; BRAF PROTEIN, HUMAN; FIZZY RELATED PROTEIN; FZR1 PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; PROTEIN KINASE INHIBITOR; UBIQUITIN PROTEIN LIGASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CARCINOGENESIS; DIMERIZATION; GENE ACTIVATION; GENE DISRUPTION; GENE INACTIVATION; GENE LOSS; GENETIC TRANSFECTION; MELANOCYTE; MOUSE; NONHUMAN; ONCOGENE RAS; PHOSPHORYLATION; PLASMID; PRIMARY CELL; PROTEIN DEGRADATION; SENESCENCE; UBIQUITINATION; ANIMAL; DRUG EFFECTS; DRUG SCREENING; GENETICS; HELA CELL LINE; HUMAN; MELANOMA; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; CARCINOGENESIS; CDH1 PROTEINS; CELL LINE, TUMOR; CYCLIN D1; DIMERIZATION; HELA CELLS; HUMANS; MELANOCYTES; MELANOMA; MICE; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85017180342     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-16-0647     Document Type: Article

References (91)

1. Pines J. Cubism and the cell cycle: the many faces of the APC/C. Nat Rev Mol Cell Biol 2011;12:427–38.
2. Manchado E, Eguren M, Malumbres M. The anaphase-promoting complex/cyclosome (APC/C): cell-cycle-dependent and -independent functions. Biochem Soc Trans 2010;38:65–71.
3. Lukas C, Sorensen CS, Kramer E, Santoni-Rugiu E, Lindeneg C, Peters JM, et al. Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex. Nature 1999;401:815–8.
4. Keck JM, Summers MK, Tedesco D, Ekholm-Reed S, Chuang LC, Jackson PK, et al. Cyclin E overexpression impair progression through mitosis by inhibiting APC(Cdh1). J Cell Biol 2007;178:371– 85.
5. Fukushima H, Ogura K, Wan L, Lu Y, Li V, Gao D, et al. SCF-mediated Cdh1 degradation defines a negative feedback system that coordinates cell-cycle progression. Cell Rep 2013;4:803–16.
6. Lau AW, Inuzuka H, Fukushima H, Wan L, Liu P, Gao D, et al. Regulation of APC(Cdh1) E3 ligase activity by the Fbw7/cyclin E signaling axis contributes to the tumor suppressor function of Fbw7. Cell Res 2013;23:947–61.
7. Peters JM. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol 2006;7:644–56.
8. Zhang J, Wan L, Dai X, Sun Y, Wei W. Functional characterization of anaphase promoting complex/cyclosome (APC/C) E3 ubiquitin ligases in tumorigenesis. Biochim Biophys Acta 2014;1845:277–93.
9. Wan L, Zou W, Gao D, Inuzuka H, Fukushima H, Berg AH, et al. Cdh1 regulates osteoblast function through an APC/C-independent modulation of Smurf1. Mol Cell 2011;44:721–33.
10. Geley S, Kramer E, Gieffers C, Gannon J, Peters JM, Hunt T. Anaphase-promoting complex/cyclosome-dependent proteolysis of human cyclin A starts at the beginning of mitosis and is not subject to the spindle assembly checkpoint. J Cell Biol 2001;153:137–48.
11. Lindon C, Pines J. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J Cell Biol 2004;164:233–41.
12. Petersen BO, Wagener C, Marinoni F, Kramer ER, Melixetian M, Lazzerini Denchi E, et al. Cell cycle- and cell growth-regulated proteolysis of mammalian CDC6 is dependent on APC-CDH1. Genes Dev 2000;14:2330–43.
13. Fujita T, Liu W, Doihara H, Wan Y. Regulation of Skp2-p27 axis by the Cdh1/anaphase-promoting complex pathway in colorectal tumorigenesis. Am J Pathol 2008;173:217–28.
14. Bassermann F, Frescas D, Guardavaccaro D, Busino L, Peschiaroli A, Pagano M. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell 2008;134:256–67.
15. Garcia-Higuera I, Manchado E, Dubus P, Canamero M, Mendez J, Moreno S, et al. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat Cell Biol 2008;10:802–11.
16. Cao J, Dai X, Wan L, Wang H, Zhang J, Goff PS, et al. The E3 ligase APC/CCdh1 promotes ubiquitylation-mediated proteolysis of PAX3 to suppress melanocyte proliferation and melanoma growth. Sci Signaling 2015;8:ra87.
17. Wellbrock C, Karasarides M, Marais R. The RAF proteins take centre stage. Nat Rev Mol Cell Biol 2004;5:875–85.
18. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature 2002;417: 949–54.
19. Roberts PJ, Der CJ. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007; 26:3291–310.
20. Bollag G, Tsai J, Zhang J, Zhang C, Ibrahim P, Nolop K, et al. Vemurafenib: the first drug approved for BRAF-mutant cancer. Nat Rev Drug Discov 2012;11:873–86.
21. Holderfield M, Deuker MM, McCormick F, McMahon M. Targeting RAF kinases for cancer therapy: BRAF-mutated melanoma and beyond. Nat Rev Cancer 2014;14:455–67.
22. Tap WD, Gong KW, Dering J, Tseng Y, Ginther C, Pauletti G, et al. Pharmacodynamic characterization of the efficacy signals due to selective BRAF inhibition with PLX4032 in malignant melanoma. Neoplasia 2010;12:637–49.
23. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford RF, Sosman J, et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 2012;367:1694–703.
24. Poulikakos PI, Rosen N. Mutant BRAF melanomas–dependence and resistance. Cancer cell 2011;19:11–5.
25. Catalanotti F, Solit DB. Will Hsp90 inhibitors prove effective in BRAF-mutant melanomas? Clin Cancer Res 2012;18:2420–2.
26. Yoshida H, Kunisada T, Kusakabe M, Nishikawa S, Nishikawa SI. Distinct stages of melanocyte differentiation revealed by anlaysis of nonuniform pigmentation patterns. Development 1996;122:1207–14.
27. Gao D, Inuzuka H, Korenjak M, Tseng A, Wu T, Wan L, et al. Cdh1 regulates cell cycle through modulating the claspin/Chk1 and the Rb/E2F1 pathways. Mol Biol Cell 2009;20:3305–16.
28. Engelbert D, Schnerch D, Baumgarten A, Wasch R. The ubiquitin ligase APC(Cdh1) is required to maintain genome integrity in primary human cells. Oncogene 2008;27:907–17.
29. Pollock PM, Harper UL, Hansen KS, Yudt LM, Stark M, Robbins CM, et al. High frequency of BRAF mutations in nevi. Nat Genet 2003;33:19–20.
30. Sackton KL, Dimova N, Zeng X, Tian W, Zhang M, Sackton TB, et al. Synergistic blockade of mitotic exit by two chemical inhibitors of the APC/C. Nature 2014;514:646–9.
31. Jacob K, Quang-Khuong DA, Jones DT, Witt H, Lambert S, Albrecht S, et al. Genetic aberrations leading to MAPK pathway activation mediate oncogene-induced senescence in sporadic pilocytic astrocy-tomas. Clin Cancer Res 2011;17:4650–60.
32. Zhu J, Woods D, McMahon M, Bishop JM. Senescence of human fibroblasts induced by oncogenic Raf. Genes Dev 1998;12:2997–3007.
33. Michaloglou C, Vredeveld LC, Soengas MS, Denoyelle C, Kuilman T, van der Horst CM, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005;436:720–4.
34. Haqq C, Nosrati M, Sudilovsky D, Crothers J, Khodabakhsh D, Pul-liam BL, et al. The gene expression signatures of melanoma progression. Proc Natl Acad Sci U S A 2005;102:6092–7.
35. Schwab M, Neutzner M, Mocker D, Seufert W. Yeast Hct1 recognizes the mitotic cyclin Clb2 and other substrates of the ubiquitin ligase APC. EMBO J 2001;20:5165–75.
36. Barrett SD, Bridges AJ, Dudley DT, Saltiel AR, Fergus JH, Flamme CM, et al. The discovery of the benzhydroxamate MEK inhibitors CI-1040 and PD 0325901. Bioorg Med Chem Lett 2008;18:6501–4.
37. Kraft C, Vodermaier HC, Maurer-Stroh S, Eisenhaber F, Peters JM. The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol Cell 2005;18:543–53.
38. Harper JW, Burton JL, Solomon MJ. The anaphase-promoting complex: it’s not just for mitosis any more. Genes Dev 2002;16:2179–206.
39. Miller AJ, Mihm MC Jr.Melanoma. N Engl J Med 2006;355:51–65.
40. Viros A, Sanchez-Laorden B, Pedersen M, Furney SJ, Rae J, Hogan K, et al. Ultraviolet radiation accelerates BRAF-driven melanomagenesis by targeting TP53. Nature 2014;511:478–82.
41. Liu W, Li W, Fujita T, Yang Q, Wan Y. Proteolysis of CDH1 enhances susceptibility to UV radiation-induced apoptosis. Carcinogenesis 2008;29:263–72.
42. Zhang BH, Guan KL. Activation of B-Raf kinase requires phosphorylation of the conserved residues Thr598 and Ser601. EMBO J 2000; 19:5429–39.
43. Chang L, Zhang Z, Yang J, McLaughlin SH, Barford D. Atomic structure of the APC/C and its mechanism of protein ubiquitination. Nature 2015;522:450–4.
44. Chang L, Zhang Z, Yang J, McLaughlin SH, Barford D. Molecular architecture and mechanism of the anaphase-promoting complex. Nature 2014;513:388–93.
45. Rape M, Reddy SK, Kirschner MW. The processivity of multiubiqui-tination by the APC determines the order of substrate degradation. Cell 2006;124:89–103.
46. McKay MM, Morrison DK. Integrating signals from RTKs to ERK/ MAPK. Oncogene 2007;26:3113–21.
47. Lu Y, Lee BH, King RW, Finley D, Kirschner MW. Substrate degradation by the proteasome: a single-molecule kinetic analysis. Science 2015;348:1250834.
48. Lu Y, Wang W, Kirschner MW. Specificity of the anaphase-promoting complex: a single-molecule study. Science 2015;348:1248737.
49. Poulikakos PI, Persaud Y, Janakiraman M, Kong X, Ng C, Moriceau G, et al. RAF inhibitor resistance is mediated by dimerization of aber-rantly spliced BRAF(V600E). Nature 2011;480:387–90.
50. Wan PT, Garnett MJ, Roe SM, Lee S, Niculescu-Duvaz D, Good VM, et al. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 2004;116:855–67.
51. He J, Chao WC, Zhang Z, Yang J, Cronin N, Barford D. Insights into degron recognition by APC/C coactivators from the structure of an Acm1-Cdh1 complex. Mol Cell 2013;50:649–60.
52. Arkin MR, Wells JA. Small-molecule inhibitors of protein-protein interactions: progressing towards the dream. Nat Rev Drug Discov 2004;3:301–17.
53. Hatzivassiliou G, Song K, Yen I, Brandhuber BJ, Anderson DJ, Alvarado R, et al. RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 2010;464:431–5.
54. Solit DB, Rosen N. Towards a unified model of RAF inhibitor resistance. Cancer Discov 2014;4:27–30.
55. Roskoski R Jr. RAF protein-serine/threonine kinases: structure and regulation. Biochem Biophys Res Commun 2010;399:313–7.
56. Poulikakos PI, Zhang C, Bollag G, Shokat KM, Rosen N. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wildtype BRAF. Nature 2010;464:427–30.
57. Hodis E, Watson IR, Kryukov GV, Arold ST, Imielinski M, Theurillat JP, et al. A landscape of driver mutations in melanoma. Cell 2012; 150:251–63.
58. The I, Ruijtenberg S, Bouchet BP, Cristobal A, Prinsen MB, van Mourik T, et al. Rb and FZR1/Cdh1 determine CDK4/6-cyclin D requirement in C. elegans and human cancer cells. Nat Commun 2015;6:5906.
59. Jang S, Atkins MB. Treatment of BRAF-mutant melanoma: the role of vemurafenib and other therapies. Clin Pharmacol Ther 2014;95: 24–31.
60. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 2010;363:809–19.
61. Liu P, Begley M, Michowski W, Inuzuka H, Ginzberg M, Gao D, et al. Cell-cycle-regulated activation of Akt kinase by phosphorylation at its carboxyl terminus. Nature 2014;508:541–5.
62. Fry DW, Harvey PJ, Keller PR, Elliott WL, Meade M, Trachet E, et al. Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol Cancer Ther 2004;3:1427–38.
63. Huang JN, Park I, Ellingson E, Littlepage LE, Pellman D. Activity of the APC(Cdh1) form of the anaphase-promoting complex persists until S phase and prevents the premature expression of Cdc20p. J Cell Biol 2001;154:85–94.
64. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012;2: 401–4.
65. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signaling 2013;6:pl1.
66. Tsao H, Chin L, Garraway LA, Fisher DE. Melanoma: from mutations to medicine. Genes Dev 2012;26:1131–55.
67. Garraway LA, Widlund HR, Rubin MA, Getz G, Berger AJ, Ramas-wamy S, et al. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 2005; 436:117–22.
68. Dankort D, Curley DP, Cartlidge RA, Nelson B, Karnezis AN, Damsky WE Jr., et al. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat Genet 2009;41:544–52.
69. Vredeveld LC, Possik PA, Smit MA, Meissl K, Michaloglou C, Horlings HM, et al. Abrogation of BRAFV600E-induced senescence by PI3K pathway activation contributes to melanomagenesis. Genes Dev 2012;26:1055–69.
70. Van Raamsdonk CD, Bezrookove V, Green G, Bauer J, Gaugler L, O’Brien JM, et al. Frequent somatic mutations of GNAQ in uveal melanoma and blue naevi. Nature 2009;457:599–602.
71. Garcia-Higuera I, Manchado E, Dubus P, Canamero M, Mendez J, Moreno S, et al. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat Cell Biol 2008;10:802–11.
72. Bosenberg M, Muthusamy V, Curley DP, Wang Z, Hobbs C, Nelson B, et al. Characterization of melanocyte-specific inducible Cre recombi-nase transgenic mice. Genesis 2006;44:262–7.
73. Harris ML, Pavan WJ. Postnatal lineage mapping of follicular melano-cytes with the Tyr::CreER(T) (2) transgene. Pigment Cell Melanoma Res 2013;26:269–74.
74. Dougherty MK, Muller J, Ritt DA, Zhou M, Zhou XZ, Copeland TD, et al. Regulation of Raf-1 by direct feedback phosphorylation. Mol Cell 2005;17:215–24.
75. Ramstad C, Sundvold V, Johansen HK, Lea T. cAMP-dependent protein kinase (PKA) inhibits T cell activation by phosphorylating ser-43 of raf-1 in the MAPK/ERK pathway. Cell Signal 2000;12:557–63.
76. de la Cova C, Greenwald I. SEL-10/Fbw7-dependent negative feedback regulation of LIN-45/Braf signaling in C. elegans via a conserved phosphodegron. Genes Dev 2012;26:2524–35.
77. Hong SW, Jin DH, Shin JS, Moon JH, Na YS, Jung KA, et al. Ring finger protein 149 is an E3 ubiquitin ligase active on wild-type v-Raf murine sarcoma viral oncogene homolog B1 (BRAF). J Biol Chem 2012;287:24017–25.
78. Gao D, Inuzuka H, Tseng A, Chin RY, Toker A, Wei W. Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat Cell Biol 2009;11:397–408.
79. Lin HK, Wang G, Chen Z, Teruya-Feldstein J, Liu Y, Chan CH, et al. Phosphorylation-dependent regulation of cytosolic localization and oncogenic function of Skp2 by Akt/PKB. Nat Cell Biol 2009;11: 420–32.
80. Mailand N, Diffley JF. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell 2005;122:915–26.
81. Sivakumar S, Gorbsky GJ. Spatiotemporal regulation of the anaphase-promoting complex in mitosis. Nat Rev Mol Cell Biol 2015;16:82–94.
82. Ungureanu D, Saharinen P, Junttila I, Hilton DJ, Silvennoinen O. Regulation of Jak2 through the ubiquitin-proteasome pathway involves phosphorylation of Jak2 on Y1007 and interaction with SOCS-1. Mol Cell Biol 2002;22:3316–26.
83. Cao J, Wan L, Hacker E, Dai X, Lenna S, Jimenez-Cervantes C, et al. MC1R is a potent regulator of PTEN after UV exposure in melano-cytes. Mol Cell 2013;51:409–22.
84. Dunham WR, Klein SB, Rhodes LM, Marcelo CL. Oleic acid and linoleic acid are the major determinants of changes in keratinocyte plasma membrane viscosity. J Invest Dermatol 1996;107:332–5.
85. Ghosh S, Rosenthal R, Zajac P, Weber WP, Oertli D, Heberer M, et al. Culture of melanoma cells in 3-dimensional architectures results in impaired immunorecognition by cytotoxic T lymphocytes specific for Melan-A/MART-1 tumor-associated antigen. Ann Surg 2005;242:851–7, discussion 8.
86. Boehm JS, Hession MT, Bulmer SE, Hahn WC. Transformation of human and murine fibroblasts without viral oncoproteins. Mol Cell Biol 2005;25:6464–74.
87. Banito A, Rashid ST, Acosta JC, Li S, Pereira CF, Geti I, et al. Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev 2009;23:2134–9.
88. Wan L, Tan M, Yang J, Inuzuka H, Dai X, Wu T, et al. APC(Cdc20) suppresses apoptosis through targeting Bim for ubiquitination and destruction. Dev Cell 2014;29:377–91.
89. Wu T, Merbl Y, Huo Y, Gallop JL, Tzur A, Kirschner MW. UBE2S drives elongation of K11-linked ubiquitin chains by the anaphasepromoting complex. Proc Natl Acad Sci U S A 2010;107:1355–60.
90. Wei W, Ayad NG, Wan Y, Zhang GJ, Kirschner MW, Kaelin WG Jr. Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 2004;428:194–8.
91. Song MS, Carracedo A, Salmena L, Song SJ, Egia A, Malumbres M, et al. Nuclear PTEN regulates the APC-CDH1 tumor-suppressive complex in a phosphatase-independent manner. Cell 2011;144:187–99.