Negative regulation of HIF-1α by an FBW7-mediated degradation pathway during hypoxia

Journal of Cellular Biochemistry

Volumn 112, Issue 12, 2011, Pages 3882-3890

  Cassavaugh, Jessica M ^a   Hale, Sarah A ^a   Wellman, Theresa L ^a   Howe, Alan K ^a   Wong, Cheung ^a,b   Lounsbury, Karen M ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

AKT; angiogenesis; endothelial cells; ovarian cancer; transcription factor; ubiquitination

Indexed keywords

BETA TUBULIN; F BOX PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEIN FBW7; UNCLASSIFIED DRUG;

ANGIOGENESIS; ARTICLE; CELL MATURATION; CELL STRAIN HEK293; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOPRECIPITATION; OVARY CANCER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; UBIQUITINATION;

CELL CYCLE PROTEINS; CELL HYPOXIA; CELL LINE, TUMOR; F-BOX PROTEINS; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; OVARIAN NEOPLASMS; PHOSPHORYLATION; PROTEOLYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 80055019700     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23321     Document Type: Article

References (41)

1. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R,. 1997. β-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16: 3797-3804.
2. Bae S-H, Jeong J-W, Park JA, Kim S-H, Bae M-K, Choi S-J, Kim K-W,. 2004. Sumoylation increases HIF-1α stability and its transcriptional activity. Biochem Biophys Res Commun 324: 394-400. (Pubitemid 39311508)
3. Balamurugan K, Wang JM, Tsai HH, Sharan S, Anver M, Leighty R, Sterneck E,. 2010. The tumour suppressor C/EBPÎ inhibits FBXW7 expression and promotes mammary tumour metastasis. EMBO J 29: 4106-4117.
4. Berta MA, Mazure N, Hattab M, Pouyssegur J, Brahimi-Horn MC,. 2007. SUMOylation of hypoxia-inducible factor-1α reduces its transcriptional activity. Biochem Biophys Res Commun 360: 646-652. (Pubitemid 47048148)
5. Bikfalvi A, Bicknell R,. 2002. Recent advances in angiogenesis, anti-angiogenesis and vascular targeting. Trends Pharmacol Sci 23: 576-582. (Pubitemid 35375803)
6. Cao Q, Lu X, Feng YJ,. 2006. Glycogen synthase kinase-3beta positively regulates the proliferation of human ovarian cancer cells. Cell Res 16: 671-677. (Pubitemid 44091443)
7. Carbia-Nagashima A, Gerez J, Perez-Castro C, Paez-Pereda M, Silberstein S, Stalla GK, Holsboer F, Arzt E,. 2007. RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1α during hypoxia. Cell 131: 309-323. (Pubitemid 47592916)
8. Cassavaugh J, Lounsbury KM,. 2011. Hypoxia-mediated biological control. J Cell Biochem 112: 735-744.
9. Crusio KM, King B, Reavie LB, Aifantis I,. 2010. The ubiquitous nature of cancer: The role of the SCF(Fbw7) complex in development and transformation. Oncogene 29: 4865-4873.
10. Dong Y, Lee SO, Zhang H, Marshall J, Gao AC, Ip C,. 2004. Prostate specific antigen expression is down-regulated by selenium through disruption of androgen receptor signaling. Cancer Res 64: 19-22. (Pubitemid 38114075)
11. Fang J, Xia C, Cao Z, Zheng JZ, Reed E, Jiang B-H,. 2005. Apigenin inhibits VEGF and HIF-1 expression via PI3K/AKT/p70S6K1 and HDM2/p53 pathways. FASEB J 19: 342-353. (Pubitemid 40316522)
12. Flugel D, Gorlach A, Michiels C, Kietzmann T,. 2007. Glycogen synthase kinase 3 phosphorylates hypoxia-inducible factor 1α and mediates its destabilization in a VHL-independent manner. Mol Cell Biol 27: 3253-3265. (Pubitemid 46685205)
13. Folkman J,. 2001. Angiogenesis-dependent diseases. Semin Oncol 28: 536-542. (Pubitemid 33134412)
14. Fuchs SY, Spiegelman VS, Suresh Kumar KG,. 2004. The many faces of βTrCP E3 ubiquitin ligases: Reflections in the magic mirror of cancer. Oncogene 23: 2028-2036. (Pubitemid 38496732)
15. Goode EL, Maurer MJ, Sellers TA, Phelan CM, Kalli KR, Fridley BL, Vierkant RA, Armasu SM, White KL, Keeney GL, Cliby WA, Rider DN, Kelemen LE, Jones MB, Peethambaram PP, Lancaster JM, Olson JE, Schildkraut JM, Cunningham JM, Hartmann LC,. 2010. Inherited determinants of ovarian cancer survival. Clin Cancer Res 16: 995-1007.
16. Gregory MA, Qi Y, Hann SR,. 2003. Phosphorylation by glycogen synthase kinase-3 controls c-myc proteolysis and subnuclear localization. J Biol Chem 278: 51606-51612. (Pubitemid 38020405)
17. Grim JE, Gustafson MP, Hirata RK, Hagar AC, Swanger J, Welcker M, Hwang HC, Ericsson J, Russell DW, Clurman BE,. 2008. Isoform- and cell cycle-dependent substrate degradation by the Fbw7 ubiquitin ligase. J Cell Biol 181: 913-920. (Pubitemid 351846825)
18. Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A,. 1998. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J 17: 1371-1384. (Pubitemid 28105516)
19. Inna MY, Vadim VS,. 2003. S-nitrosation of Cys-800 of HIF-1alpha protein activates its interaction with p300 and stimulates its transcriptional activity. FEBS Lett 549: 105-109.
20. 2 sensing. Science 292: 464-468. (Pubitemid 32335941)
21. Jokilehto T, Jaakkola PM,. 2010. The role of HIF prolyl hydroxylases in tumour growth. J Cell Mol Med 14: 758-770.
22. Li F, Sonveaux P, Rabbani ZN, Liu S, Yan B, Huang Q, Vujaskovic Z, Dewhirst MW, Li C-Y,. 2007. Regulation of HIF-1α stability through S-nitrosylation. Mol Cell 26: 63-74. (Pubitemid 46550936)
23. Liao D, Johnson R,. 2007. Hypoxia: A key regulator of angiogenesis in cancer. Cancer Metastasis Rev 26: 281-290. (Pubitemid 47101669)
24. Lounsbury KM, Beddow AL, Macara IG,. 1994. A family of proteins that stabilize the Ran/TC4 GTPase in its GTP-bound conformation. J Biol Chem 269: 11285-11290. (Pubitemid 24200340)
25. Manning BD, Cantley LC,. 2007. AKT/PKB signaling: Navigating downstream. Cell 129: 1261-1274. (Pubitemid 46962095)
26. Mao JH, Kim IJ, Wu D, Climent J, Kang HC, DelRosario R, Balmain A,. 2008. FBXW7 targets mTOR for degradation and cooperates with PTEN in tumor suppression. Science 321: 1499-1502.
27. McGonigle KF, Muntz HG, Vuky J, Paley PJ, Veljovich DS, Greer BE, Goff BA, Gray HJ, Malpass TW,. 2011. Combined weekly topotecan and biweekly bevacizumab in women with platinum-resistant ovarian, peritoneal, or fallopian tube cancer: Results of a phase 2 study. Cancer 117: 3731-3740.
28. Min J-H, Yang H, Ivan M, Gertler F, Kaelin WG, Jr., Pavletich NP,. 2002. Structure of an HIF-1alpha-pVHL complex: Hydroxyproline recognition in signaling. Science 296: 1886-1889. (Pubitemid 34596278)
29. Mottet D, Dumont V, Deccache Y, Demazy C, Ninane N, Raes M, Michiels C,. 2003. Regulation of hypoxia-inducible factor-1α protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3β pathway in HepG2 cells. J Biol Chem 278: 31277-31285. (Pubitemid 36994645)
30. Mylonis I, Chachami G, Samiotaki M, Panayotou G, Paraskeva E, Kalousi A, Georgatsou E, Bonanou S, Simos G,. 2006. Identification of MAPK phosphorylation sites and their role in the localization and activity of hypoxia-inducible factor-1α. J Biol Chem 281: 33095-33106. (Pubitemid 46043259)
31. Nikolakaki E, Coffer PJ, Hemelsoet R, Woodgett JR, Defize LH,. 1993. Glycogen synthase kinase 3 phosphorylates Jun family members in vitro and negatively regulates their transactivating potential in intact cells. Oncogene 8: 833-840. (Pubitemid 23087413)
32. Pore N, Jiang Z, Shu H-K, Bernhard E, Kao GD, Maity A,. 2006. Akt1 activation can augment hypoxia-inducible factor-1α expression by increasing protein translation through a mammalian target of rapamycin-independent pathway. Mol Cancer Res 4: 471-479. (Pubitemid 44197042)
33. Semenza GL,. 2010. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29: 625-634.
34. Skurk C, Maatz H, Rocnik E, Bialik A, Force T, Walsh K,. 2005. Glycogen-synthase kinase3beta/beta-catenin axis promotes angiogenesis through activation of vascular endothelial growth factor signaling in endothelial cells. Circ Res 96: 308-318. (Pubitemid 40279905)
35. Treins C, Giorgetti-Peraldi S, Murdaca J, Semenza GL, Van Obberghen E,. 2002. Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J Biol Chem 277: 27975-27981. (Pubitemid 34966746)
36. Welcker M, Clurman BE,. 2008. FBW7 ubiquitin ligase: A tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 8: 83-93. (Pubitemid 351161321)
37. Wertz IE, Kusam S, Lam C, Okamoto T, Sandoval W, Anderson DJ, Helgason E, Ernst JA, Eby M, Liu J, Belmont LD, Kaminker JS, O'Rourke KM, Pujara K, Kohli PB, Johnson AR, Chiu ML, Lill JR, Jackson PK, Fairbrother WJ, Seshagiri S, Ludlam MJ, Leong KG, Dueber EC, Maecker H, Huang DC, Dixit VM,. 2011. Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature 471: 110-114.
38. Wong C, Wellman TL, Lounsbury KM,. 2003. VEGF and HIF-1alpha expression are increased in advanced stages of epithelial ovarian cancer. Gynecol Oncol 91: 513-517. (Pubitemid 38388143)
39. Zhong H, De Marzo AM, Laughner E, Lim M, Hilton DA, Zagzag D, Buechler P, Isaacs WB, Semenza GL, Simons JW,. 1999. Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res 59: 5830-5835.
40. Zhong H, Chiles K, Feldser D, Laughner E, Hanrahan C, Georgescu M-M, Simons JW, Semenza GL,. 2000. Modulation of hypoxia-inducible factor 1α expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: Implications for tumor angiogenesis and therapeutics. Cancer Res 60: 1541-1545. (Pubitemid 30183422)
41. Zhong X-S, Zheng JZ, Reed E, Jiang B-H,. 2004. SU5416 inhibited VEGF and HIF-1α expression through the PI3K/AKT/p70S6K1 signaling pathway. Biochem Biophys Res Commun 324: 471-480. (Pubitemid 39345542)