Β-arrestin1 mediates metastatic growth of breast cancer cells by facilitating HIF-1-dependent VEGF expression

Oncogene

Volumn 31, Issue 3, 2012, Pages 282-292

  Shenoy, S K ^a   Han, S ^a   Zhao, Y L ^a   Hara, M R ^a   Oliver, T ^a   Cao, Y ^a   Dewhirst, M W ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

arrestin; HIF 1; hypoxia; VEGF

Indexed keywords

BETA ARRESTIN 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMATINIB; OXYGEN; THALIDOMIDE; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER GROWTH; CARCINOMA CELL; CELL HYPOXIA; CELL SURVIVAL; CELL VIABILITY; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; INTRACELLULAR SIGNALING; INTRADUCTAL CARCINOMA; INVASIVE CARCINOMA; METASTASIS; MOUSE; NONHUMAN; NUCLEAR EXPORT; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TRANSCRIPTION REGULATION; UPREGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, NUDE; NEOPLASM METASTASIS; PIPERAZINES; PROTEIN STABILITY; PYRIMIDINES; THALIDOMIDE; TRANSCRIPTION, GENETIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MUS MUSCULUS;

EID: 84855927182     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.238     Document Type: Article

References (48)

1. Alvarez CJ, Lodeiro M, Theodoropoulou M, Camina JP, Casanueva FF, Pazos Y. (2009). Obestatin stimulates Akt signalling in gastric cancer cells through beta-arrestin-mediated epidermal growth factor receptor transactivation. Endocr Relat Cancer 16: 599-611.
2. Arany Z, Huang LE, Eckner R, Bhattacharya S, Jiang C, Goldberg MA et al. (1996). An essential role for p300/CBP in the cellular response to hypoxia. Proc Natl Acad Sci USA 93: 12969-12973. (Pubitemid 26382753)
3. Attramadal H, Arriza JL, Aoki C, Dawson TM, Codina J, Kwatra MM et al. (1992). Beta-arrestin2, a novel member of the arrestin/beta-arrestin gene family. J Biol Chem 267: 17882-17890.
4. Beppu K, Jaboine J, Merchant MS, Mackall CL, Thiele CJ. (2004). Effect of imatinib mesylate on neuroblastoma tumorigenesis and vascular endothelial growth factor expression. J Natl Cancer Inst 96: 46-55. (Pubitemid 38180959)
5. Buchanan FG, Gorden DL, Matta P, Shi Q, Matrisian LM, DuBois RN. (2006). Role of beta-arrestin 1 in the metastatic progression of colorectal cancer. Proc Natl Acad Sci USA 103: 1492-1497. (Pubitemid 43191193)
6. Chuaqui RF, Zhuang Z, Emmert-Buck MR, Liotta LA, Merino MJ. (1997). Analysis of loss of heterozygosity on chromosome 11q13 in atypical ductal hyperplasia and in situ carcinoma of the breast. Am J Pathol 150: 297-303. (Pubitemid 27027118)
7. D'Amato RJ, Loughnan MS, Flynn E, Folkman J. (1994). Thalidomide is an inhibitor of angiogenesis. Proc Natl Acad Sci USA 91: 4082-4085. (Pubitemid 24139577)
8. Daaka Y. (2004). G proteins in cancer: the prostate cancer paradigm. Sci STKE 2004: re2.
9. Dasgupta P, Rastogi S, Pillai S, Ordonez-Ercan D, Morris M, Haura E et al. (2006). Nicotine induces cell proliferation by beta-arrestinmediated activation of Src and Rb-Raf-1 pathways. J Clin Invest 116: 2208-2217. (Pubitemid 44162330)
10. DeWire SM, Ahn S, Lefkowitz RJ, Shenoy SK. (2007). Beta-arrestins and cell signaling. Annu Rev Physiol 69: 483-510.
11. Dredge K, Marriott JB, Macdonald CD, Man HW, Chen R, Muller GW et al. (2002). Novel thalidomide analogues display antiangiogenic activity independently of immunomodulatory effects. Br J Cancer 87: 1166-1172. (Pubitemid 35418112)
12. Ebos JM, Tran J, Master Z, Dumont D, Melo JV, Buchdunger E et al. (2002). Imatinib mesylate (STI-571) reduces Bcr-Abl-mediated vascular endothelial growth factor secretion in chronic myelogenous leukemia. Mol Cancer Res 1: 89-95. (Pubitemid 36306767)
13. Ferrara N, Gerber HP, LeCouter J. (2003). The biology of VEGF and its receptors. Nat Med 9: 669-676. (Pubitemid 36749215)
14. Figg WD. (2006). The 2005 Leon I. Goldberg Young Investigator Award Lecture: development of thalidomide as an angiogenesis inhibitor for the treatment of androgen-independent prostate cancer. Clin Pharmacol Ther 79: 1-8. (Pubitemid 43069573)
15. Folkman J, Merler E, Abernathy C, Williams G. (1971). Isolation of a tumor factor responsible for angiogenesis. J Exp Med 133: 275-288.
16. Gavard J, Gutkind JS. (2006). VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 8: 1223-1234. (Pubitemid 44660587)
17. Ge L, Shenoy SK, Lefkowitz RJ, DeFea K. (2004). Constitutive protease-activated receptor-2-mediated migration of MDA MB-231 breast cancer cells requires both beta-arrestin-1 and-2. J Biol Chem 279: 55419-55424. (Pubitemid 40066542)
18. Girnita L, Shenoy SK, Sehat B, Vasilcanu R, Vasilcanu D, Girnita A et al. (2007). Beta-arrestin and Mdm2 mediate IGF-1 receptorstimulated ERK activation and cell cycle progression. J Biol Chem 282: 11329-11338. (Pubitemid 47100796)
19. Holaday JW, Berkowitz BA. (2009). Antiangiogenic drugs: insights into drug development from endostatin, avastin and thalidomide. Mol Interv 9: 157-166.
20. Kang J, Shi Y, Xiang B, Qu B, Su W, Zhu M et al. (2005). A nuclear function of beta-arrestin1 in GPCR signaling: regulation of histone acetylation and gene transcription. Cell 123: 833-847. (Pubitemid 41721030)
21. Kelly P, Moeller BJ, Juneja J, Booden MA, Der CJ, Daaka Y et al. (2006). The G12 family of heterotrimeric G proteins promotes breast cancer invasion and metastasis. Proc Natl Acad Sci USA 103: 8173-8178. (Pubitemid 43801071)
22. Kohout TA, Lin FS, Perry SJ, Conner DA, Lefkowitz RJ. (2001). beta-Arrestin 1 and 2 differentially regulate heptahelical receptor signaling and trafficking. Proc Natl Acad Sci USA 98: 1601-1606. (Pubitemid 32165545)
23. Kvietikova I, Wenger RH, Marti HH, Gassmann M. (1995). The transcription factors ATF-1 and CREB-1 bind constitutively to the hypoxia-inducible factor-1 (HIF-1) DNA recognition site. Nucleic Acids Res 23: 4542-4550. (Pubitemid 126003251)
24. Lakshmikanthan V, Zou L, Kim JI, Michal A, Nie Z, Messias NC et al. (2009). Identification of betaArrestin2 as a corepressor of androgen receptor signaling in prostate cancer. Proc Natl Acad Sci USA 106: 9379-9384.
25. Lal A, Haynes SR, Gorospe M. (2005). Clean western blot signals from immunoprecipitated samples. Mol Cell Probes 19: 385-388. (Pubitemid 41586134)
26. Lefkowitz RJ, Rajagopal K, Whalen EJ. (2006). New roles for betaarrestins in cell signaling: not just for seven-transmembrane receptors. Mol Cell 24: 643-652. (Pubitemid 44839219)
27. Lefkowitz RJ, Shenoy SK. (2005). Transduction of receptor signals by beta-arrestins. Science 308: 512-517.
28. Letessier A, Sircoulomb F, Ginestier C, Cervera N, Monville F, Gelsi-Boyer V et al. (2006). Frequency, prognostic impact, and subtype association of 8p12, 8q24, 11q13, 12p13, 17q12, and 20q13 amplifications in breast cancers. BMC Cancer 6: 245.
29. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. (1989). Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306-1309. (Pubitemid 20066716)
30. Li TT, Alemayehu M, Aziziyeh AI, Pape C, Pampillo M, Postovit LM et al. (2009). Beta-arrestin/Ral signaling regulates lysophosphatidic acid-mediated migration and invasion of human breast tumor cells. Mol Cancer Res 7: 1064-1077.
31. Liu Y, Cox SR, Morita T, Kourembanas S. (1995). Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 50 enhancer. Circ Res 77: 638-643.
32. Ma XJ, Salunga R, Tuggle JT, Gaudet J, Enright E, McQuary P et al. (2003). Gene expression profiles of human breast cancer progression. Proc Natl Acad Sci USA 100: 5974-5979. (Pubitemid 36576916)
33. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME et al. (1999). The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275. (Pubitemid 29246458)
34. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD et al. (2005). Genes that mediate breast cancer metastasis to lung. Nature 436: 518-524. (Pubitemid 41112921)
35. Moeller BJ, Cao Y, Li CY, Dewhirst MW. (2004). Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 5: 429-441. (Pubitemid 38610245)
36. Mythreye K, Blobe GC. (2009). The type III TGF-beta receptor regulates epithelial and cancer cell migration through beta-arrestin2-mediated activation of Cdc42. Proc Natl Acad Sci USA 106: 8221-8226.
37. Niida A, Smith AD, Imoto S, Aburatani H, Zhang MQ, Akiyama T. (2009). Gene set-based module discovery in the breast cancer transcriptome. BMC Bioinformatics 10: 71.
38. Raghuwanshi SK, Nasser MW, Chen X, Strieter RM, Richardson RM. (2008). Depletion of beta-arrestin-2 promotes tumor growth and angiogenesis in a murine model of lung cancer. J Immunol 180: 5699-5706.
39. Rosano L, Cianfrocca R, Masi S, Spinella F, Di Castro V, Biroccio A et al. (2009). Beta-arrestin links endothelin A receptor to betacatenin signaling to induce ovarian cancer cell invasion and metastasis. Proc Natl Acad Sci USA 106: 2806-2811.
40. Scott MG, Le Rouzic E, Perianin A, Pierotti V, Enslen H, Benichou S et al. (2002). Differential nucleocytoplasmic shuttling of betaarrestins. Characterization of a leucine-rich nuclear export signal in beta-arrestin2. J Biol Chem 277: 37693-37701.
41. Semenza GL. (2007). Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007: cm8.
42. Shenoy SK, Xiao K, Venkataramanan V, Snyder PM, Freedman NJ, Weissman AM. (2008). Nedd4 mediates agonist-dependent ubiquitination, lysosomal targeting, and degradation of the beta2-adrenergic receptor. J Biol Chem 283: 22166-22176.
43. Vacca A, Scavelli C, Montefusco V, Di Pietro G, Neri A, Mattioli M et al. (2005). Thalidomide downregulates angiogenic genes in bone marrow endothelial cells of patients with active multiple myeloma. J Clin Oncol 23: 5334-5346. (Pubitemid 46206987)
44. Vlahovic G, Rabbani ZN, Herndon II JE, Dewhirst MW, Vujaskovic Z. (2006). Treatment with Imatinib in NSCLC is associated with decrease of phosphorylated PDGFR-beta and VEGF expression, decrease in interstitial fluid pressure and improvement of oxygenation. Br J Cancer 95: 1013-1019. (Pubitemid 44606827)
45. Wang GL, Jiang BH, Rue EA, Semenza GL. (1995). Hypoxiainducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 92: 5510-5514.
46. Wang GL, Semenza GL. (1995). Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270: 1230-1237.
47. Wang P, Wu Y, Ge X, Ma L, Pei G. (2003). Subcellular localization of beta-arrestins is determined by their intact N domain and the nuclear export signal at the C terminus. J Biol Chem 278: 11648-11653. (Pubitemid 36792727)
48. Zou L, Yang R, Chai J, Pei G. (2008). Rapid xenograft tumor progression in beta-arrestin1 transgenic mice due to enhanced tumor angiogenesis. FASEB J 22: 355-364. (Pubitemid 351227345)