FBW7 regulates endothelial functions by targeting KLF2 for ubiquitination and degradation

Cell Research

Volumn 23, Issue 6, 2013, Pages 803-819

  Wang, Rui ^a,c   Wang, Yan ^a   Liu, Ning ^a,d   Ren, Chunguang ^b   Jiang, Cong ^a   Zhang, Kai ^a   Yu, Su ^a   Chen, Yunfei ^a   Tang, Hui ^a   Deng, Qi ^a   Fu, Cong ^b   Wang, Yingcong ^a   Li, Rong ^a   Liu, Mingyao ^a   Pan, Weijun ^b   Wang, Ping ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c LIAOCHENG UNIVERSITY   (China)

^d HANGZHOU NORMAL UNIVERSITY   (China)

Author keywords

Angiogenesis; Cell migration; Degradation; FBW7; KLF2; Ubiquitin

Indexed keywords

CELL CYCLE PROTEIN; F BOX PROTEIN; FBXW7 PROTEIN, HUMAN; GLYCOGEN SYNTHASE KINASE 3; KLF2 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE;

ANGIOGENESIS; ANIMAL; ARTICLE; CELL DIFFERENTIATION; CELL LINE; CELL MOTION; ENDOTHELIUM; GENETICS; HUMAN; INFLAMMATION; METABOLISM; MOUSE; PHOSPHORYLATION; PRENATAL DEVELOPMENT; RNA INTERFERENCE; UBIQUITINATION; UMBILICAL VEIN ENDOTHELIAL CELL; ZEBRA FISH;

ANIMALS; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL LINE; CELL MOVEMENT; ENDOTHELIUM; F-BOX PROTEINS; GLYCOGEN SYNTHASE KINASE 3; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; RNA INTERFERENCE; RNA, SMALL INTERFERING; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; ZEBRAFISH;

DANIO RERIO;

EID: 84878728282     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2013.42     Document Type: Article

References (59)

1. Lee S, Chen TT, Barber CL, et al. Autocrine VEGF signaling is required for vascular homeostasis. Cell 2007; 130:691-703.
2. Fadini GP, Agostini C, Sartore S, Avogaro A. Endothelial progenitor cells in the natural history of atherosclerosis. Atherosclerosis 2007; 194:46-54.
3. Folkman J. Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 2007; 6:273-286.
4. Rao RM, Yang L, Garcia-Cardena G, Luscinskas FW. Endothelial- dependent mechanisms of leukocyte recruitment to the vascular wall. Cir Res 2007; 101:234-247.
5. Sakao S, Tatsumi K, Voelkel NF. Endothelial cells and pulmonary arterial hypertension: apoptosis, proliferation, interaction and transdifferentiation. Respir Res 2009; 10:95.
6. McConnell BB, Yang VW. Mammalian Kruppel-like factors in health and diseases. Physiol Rev 2010; 90:1337-1381.
7. Nayak L, Lin Z, Jain MK. "Go with the flow": how Kruppellike factor 2 regulates the vasoprotective effects of shear stress. Antioxid Redox Signal 2011; 15:1449-1461.
8. Garrido-Martin EM, Blanco FJ, Roque M, et al. Vascular injury triggers Krüppel-like factor 6 mobilization and cooperation with Sp1 to promote endothelial activation through upregulation of the activin receptor-like kinase 1 gene. Cir Res 2013; 112:113-127.
9. Yang DH, Hsu CF, Lin CY, Guo JY, Yu WC, Chang VH. Krüppel-like factor 10 upregulates the expression of cyclooxygenase 1 and further modulates angiogenesis in endothelial cell and platelet aggregation in gene-deficient mice. Int J Biochem Cell Biol 2012; 45:419-428.
10. Helbing T, Volkmar F, Goebel U, et al. Kruppel-like factor 15 regulates BMPER in endothelial cells. Cardiovasc Res 2010; 85:551-559.
11. Zhou G, Hamik A, Nayak L, et al. Endothelial Krüppel-like factor 4 protects against atherothrombosis in mice. J Clin Invest 2012; 122:4727-4731.
12. Nicoli S, Standley C, Walker P, Hurlstone A, Fogarty KE, Lawson ND. MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature 2010; 464:1196-1200.
13. Lin Z, Natesan V, Shi H, et al. Krüppel-like factor 2 regulates endothelial barrier function. Arterioscler Thromb Vasc Biol 2010; 30:1952-1959.
14. Bhattacharya R, Senbanerjee S, Lin Z, et al. Inhibition of vascular permeability factor/vascular endothelial growth factormediated angiogenesis by the Kruppel-like factor KLF2. J Biol Chem 2005; 280:28848-28851.
15. SenBanerjee S, Lin Z, Atkins GB, et al. KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation. J Exp Med 2004; 199:1305-1315.
16. Crusio KM, King B, Reavie LB, Aifantis I. The ubiquitous nature of cancer: the role of the SCF(Fbw7) complex in development and transformation. Oncogene 2010; 29:4865- 4873.
17. Wang W, Ha CH, Jhun BS, Wong C, Jain MK, Jin ZG. Fluid shear stress stimulates phosphorylation-dependent nuclear export of HDAC5 and mediates expression of KLF2 and eNOS. Blood 2010; 115:2971-2979.
18. Sen-Banerjee S, Mir S, Lin Z, et al. Krüppel-like factor 2 as a novel mediator of statin effects in endothelial cells. Circulation 2005; 112:720-726.
19. Wu W, Xiao H, Laguna-Fernandez A, et al. Flow-dependent regulation of Krüppel-like factor 2 is mediated by microRNA- 92a. Circulation 2011; 124:633-641.
20. Hiroi T, Deming CB, Zhao H, et al. Proteasome inhibitors enhance endothelial thrombomodulin expression via induction of Krüppel-like transcription factors. Arterioscler Thromb Vasc Biol 2009; 29:1587-1593.
21. Welcker M, Clurman BE. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 2008; 8:83-93.
22. Wang Z, Inuzuka H, Zhong J, et al. Tumor suppressor functions of FBW7 in cancer development and progression. FEBS Lett 2012; 586:1409-1418.
23. Liu N, Li H, Li S, et al. The Fbw7/human CDC4 tumor suppressor targets proproliferative factor KLF5 for ubiquitination and degradation through multiple phosphodegron motifs. J Biol Chem 2010; 285:18858-18867.
24. Wang Z, Inuzuka H, Fukushima H, et al. Emerging roles of the FBW7 tumour suppressor in stem cell differentiation. EMBO Rep 2012; 13:36-43.
25. Hoeck JD, Jandke A, Blake SM, et al. Fbw7 controls neural stem cell differentiation and progenitor apoptosis via Notch and c-Jun. Nat Neurosci 2010; 13:1365-1372.
26. Reavie L, Della Gatta G, Crusio K, et al. Regulation of hematopoietic stem cell differentiation by a single ubiquitin ligasesubstrate complex. Nat Immunol 2010; 11:207-215.
27. Matsumoto A, Onoyama I, Sunabori T, Kageyama R, Okano H, Nakayama KI. Fbxw7-dependent degradation of Notch is required for control of "stemness" and neuronal-glial differentiation in neural stem cells. J Biol Chem 2011; 286:13754- 13764.
28. Tetzlaff MT, Yu W, Li M, et al. Defective cardiovascular development and elevated cyclin E and Notch proteins in mice lacking the Fbw7 F-box protein. Proc Natl Acad Sci USA 2004; 101:3338-3345.
29. Flugel D, Gorlach A, Kietzmann T. GSK-3β regulates cell growth, migration, and angiogenesis via Fbw7 and USP28- dependent degradation of HIF-1α. Blood 2012; 119:1292- 1301.
30. Tan M, Zhao Y, Kim SJ, 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.
31. Izumi N, Helker C, Ehling M, Behrens A, Herzog W, Adams RH. Fbxw7 controls angiogenesis by regulating endothelial notch activity. PloS One 2012; 7:e41116.
32. Spruck CH, Strohmaier H, Sangfelt O, et al. hCDC4 gene mutations in endometrial cancer. Cancer Res 2002; 62:4535- 4539.
33. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 2006; 7:359-371.
34. Carlson CM, Endrizzi BT, Wu J, et al. Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature 2006; 442:299-302.
35. Williams CK, Li JL, Murga M, Harris AL, Tosato G. Upregulation of the Notch ligand Delta-like 4 inhibits VEGFinduced endothelial cell function. Blood 2006; 107:931-939.
36. Welcker M, Clurman BE. Fbw7/hCDC4 dimerization regulates its substrate interactions. Cell Div 2007; 2:7.
37. Sako K, Fukuhara S, Minami T, et al. Angiopoietin-1 induces Krüppel-like factor 2 expression through a phosphoinositide 3-kinase/AKT-dependent activation of myocyte enhancer factor 2. J Biol Chem 2009; 284:5592-5601.
38. Li Z, Huang H, Boland P, et al. Embryonic stem cell tumor model reveals role of vascular endothelial receptor tyrosine phosphatase in regulating Tie2 pathway in tumor angiogenesis. Proc Natl Acad Sci USA 2009; 106:22399-22404.
39. Lu CW, Yabuuchi A, Chen L, Viswanathan S, Kim K, Daley GQ. Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat Genet 2008; 40:921-926.
40. Zhang X, Srinivasan SV, Lingrel JB. WWP1-dependent ubiquitination and degradation of the lung Krüppel-like factor, KLF2. Biochem Biophys Res Commun 2004; 316:139-148.
41. Conkright MD, Wani MA, Lingrel JB. Lung Kruppel-like factor contains an autoinhibitory domain that regulates its transcriptional activation by binding WWP1, an E3 ubiquitin ligase. J Biol Chem 2001; 276:29299-29306.
42. Xie P, Tang Y, Shen S, et al. Smurf1 ubiquitin ligase targets Kruppel-like factor KLF2 for ubiquitination and degradation in human lung cancer H1299 cells. Biochem Biophys Res Commun 2011; 407:254-259.
43. Schulein C, Eilers M, Popov N. PI3K-dependent phosphorylation of Fbw7 modulates substrate degradation and activity. FEBS Lett 2011; 585:2151-2157.
44. Min SH, Lau AW, Lee TH, et al. Negative regulation of the stability and tumor suppressor function of Fbw7 by the Pin1 prolyl isomerase. Mol Cell 2012; 46:771-783.
45. Yokobori T, Mimori K, Iwatsuki M, et al. p53-Altered FBXW7 expression determines poor prognosis in gastric cancer cases. Cancer Res 2009; 69:3788-3794.
46. Mao JH, Perez-Losada J, Wu D, et al. Fbxw7/Cdc4 is a p53- dependent, haploinsufficient tumour suppressor gene. Nature 2004; 432:775-779.
47. Stempien-Otero A, Karsan A, Cornejo CJ, et al. Mechanisms of hypoxia-induced endothelial cell death. Role of p53 in apoptosis. J Biol Chem 1999; 274:8039-8045.
48. Welcker M, Orian A, Grim JE, Eisenman RN, Clurman BE. A nucleolar isoform of the Fbw7 ubiquitin ligase regulates c- Myc and cell size. Curr Biol 2004; 14:1852-1857.
49. Zhao D, Zheng HQ, Zhou Z, Chen C. The Fbw7 tumor suppressor targets KLF5 for ubiquitin-mediated degradation and suppresses breast cell proliferation. Cancer Res 2010; 70:4728-4738.
50. Bhaskaran N, van Drogen F, Ng HF, et al. Fbw7alpha and fbw7gamma collaborate to shuttle cyclin e1 into the nucleolus for multiubiquitylation. Mol Cell Biol 2013; 33:85-97.
51. Busino L, Millman SE, Scotto L, et al. Fbxw7α- and GSK3- mediated degradation of p100 is a pro-survival mechanism in multiple myeloma. Nat Cell Biol 2012; 14:375-385.
52. Biswas M, Phan D, Watanabe M, Chan JY. The Fbw7 tumor suppressor regulates nuclear factor E2-related factor 1 transcription factor turnover through proteasome-mediated proteolysis. J Biol Chem 2011; 286:39282-39289.
53. Tsunematsu R, Nakayama K, Oike Y, et al. Mouse Fbw7/Sel- 10/Cdc4 is required for notch degradation during vascular development. J Biol Chem 2004; 279:9417-9423.
54. Lidington EA, Moyes DL, McCormack AM, Rose ML. A comparison of primary endothelial cells and endothelial cell lines for studies of immune interactions. Transpl Immunol 1999; 7:239-246.
55. Mao JH, Kim IJ, Wu D, et al. FBXW7 targets mTOR for degradation and cooperates with PTEN in tumor suppression. Science 2008; 321:1499-1502.
56. Vermot J, Forouhar AS, Liebling M, et al. Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biol 2009; 7:e1000246.
57. Yokobori T, Mimori K, Iwatsuki M, et al. Copy number loss of FBXW7 is related to gene expression and poor prognosis in esophageal squamous cell carcinoma. Int J Oncol 2012; 41:253-259.
58. Fu YF, Du TT, Dong M, et al. Mir-144 selectively regulates embryonic alpha-hemoglobin synthesis during primitive erythropoiesis. Blood 2009; 113:1340-1349.
59. Pan W, Pham VN, Stratman AN, et al. CDP-diacylglycerol synthetase-controlled phosphoinositide availability limits VEGFA signaling and vascular morphogenesis. Blood 2012; 120:489-498.